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i^l^fl^^^  cjg. 


THE  EUSPORANGIATAE 

THE  COMPARATIVE  MORPHOLOGY 

OF  THE  OPHIOGLOSSACEAE 

AND  MARATTIACEAE 


BY 
DOUGLAS    HOUGHTON   CAMPBELL 

PROFESSOR    OF    BOTANY,    LELAND  STANFORD   JUNIOR   UNIVERSITY 


WASHINGTON,  D.  C. 

Published  by  the  Carnei^ie  Institution  of  Wasiiinjj;ton 

1911 


CARNEGIE    INSTITUTION    OF  WASHINGTON 
Publication  No.   140 


Copies  of  this  Book 
wertt  first  issued 

Allb2919n 


PRESS    OF   ISAAC    H.    BLANCHARD    COMPANY 
NEW    YORK 


PREFACE. 

The  great  importance  of  the  eusporangiate  ferns  as  the  nearest  existing  rela- 
tives of  the  Paleozoic  ancestors  of  the  higher  types  of  Hovvcring  plants  invests 
them  with  an  especial  interest  tor  the  student  of  plant  evolution;  and  no  apology 
is  necessary  for  presenting  at  length  a  summary  of  our  present  knowledge  of  the 
structure  and  development  of  these  important  plants. 

For  more  than  twenty  years  the  writer  has  been  much  interested  in  the  study 
of  the  Eusporangiatre  and  during  this  time  has  published  a  number  of  works  deal- 
ing with  them.  He  has  had  rather  unusual  opportunities  for  collecting  these  forms, 
and  an  extensive  and  representative  collection  of  materials  comprising  a  good  many 
species  has  been  accumulated,  so  that  the  time  seemed  ripe  for  a  comparative  study 
of  the  group,  for  the  purpose  of  determining,  as  far  as  might  be,  the  relationships 
existing  between  the  different  genera,  as  well  as  for  throwing  some  light  upon  the 
question  of  their  position  in  the  great  series  of  ferns. 

The  present  memoir  is  an  attempt  to  present  the  results  of  these  studies,  based 
mainly  upon  the  writer's  own  materials,  but  supplemented  by  a  careful  study  of 
the  work  of  other  investigators  who  have  described  the  structure  and  development 
of  the  EusporangiatsE. 

The  writer's  grateful  acknowledgments  arc  due  to  a  number  of  colleagues  who 
have  rendered  assistance  in  various  ways.  Especially  is  he  indebted  to  Prof.  E.  C. 
Jeffrey,  through  whose  kindness  a  large  number  of  admirably  preserved  prothallia 
and  young  plants  of  Botrychnim  virginimmm  were  sent  the  writer,  and  in  addition 
a  number  of  valuable  slides  of  the  same.  Without  this  material  the  work  on  5o- 
trychium  would  have  been  very  incomplete. 

To  my  colleague  in  Stanford  University,  Prof.  L.  L.  Burlingame,  thanks  are 
due  for  valuable  assistance  in  the  preparation  of  the  photographic  plates,  as  well  as 
for  the  use  of  a  number  of  important  sWAts  oi  Ophioglossum  and  Helminthostachys. 

To  Prof.  J.  C.  Willis,  of  the  Botanic  Gardens  at  Peradeniya,  the  writer  would 
express  his  appreciation  of  many  kindnesses  and  assistance  in  collecting  during  his 
stay  in  Ceylon. 

It  was  the  good  fortune  of  the  writer  to  enjoy  the  unequaled  facilities  for 
collecting  material  offered  by  the  great  gardens  at  Buitenzorg  and  Tjibodas  in  Java, 
where,  through  the  interest  and  courtesy  of  the  distinguished  director.  Professor 
M.  Treub,  whose  recent  death  was  such  an  irreparable  loss  to  science,  means  were 
afforded  for  securing  the  most  valuable  materials  used  in  the  preparation  of  the 
present  work. 

Douglas  Houghton  Campbell. 

Stanford  University,  April,  1910. 


50568 


TABLE    OF    CON'lENTS. 


Pkefack iii 

Introuuction 3-4 

PaKT    I.     Till-:    Ol'HIOGLOSSALES 

I.  Thh  (Jamhtophv,.           b-ii 

Germination  in  Ophioglossum 7 

The  Adult  Cianietophyte  of  Ophiogloisum 10 

The  Histology  of  the  Camctophyte 15 

The  Gamctophyte  of  fici^rvi/""'" 16 

The  Histology  of  the  Gametophyte  of  Z?o?,v. /"",/, 18 

The  Gametophyte  of  f/f/m;n?/(oi/ii( 7/ vx 19 

The  Endophyte 21 

The  Sexual  Organs 22 

The  Antheridium 22 

The  Antheridium  of  Of>liioglnssunt 22 

The  Antheridium  of  i?o// J. /hh/h 24 

The  Antheridium  of  Hrlnunthostiuhys 25 

Spermatogenesis 26 

The  Archegonium 28 

The  Archegonium  of  O/j/dVvf/ojjHm 28 

The  Archegonium  of  5ofr)i(7(/«m 30 

Fertilization ^I 

Fertilization  in  5o/ry(7(n/m  r;;f;H/V;HH?H 31 

Significance  of  the  Endophyte 32 

II.  The  Embryo 34-54 

The  Embryo  of  Ophioglossum 34 

The  Development  of  the  Primary  Bud  in  0/)/»oi;/oj-X!i/«  mo/wi  I  (»H("; 40 

The  Embryo  o(  Ophioglossum  vul^atum 4^ 

The  Anatomy  of  the  Young  Sporophyte  of  0/)/;/Q^/ojJum 44 

The  Embryo  of  5o^rvi7i/um 46 

The  PZmbryo  of  Hehmnthostachys 54 

in.  The  Young  Sporophyte 55-84 

The  Young  Sporophyte  of  Ophioglossum 55 

The  Young  Sporophyte  of  Botryrhium 59 

The  Young  Sporophyte  of //<7m(H(/if)jM<7n'.f 67 

Comparison  of  the  Young  Sporophytes  of  the  Ophioglossaceae 82 

IV.   The  Adult  Sporophyte 85-116 

The  Sporophyte  of  Ophioglossum 86 

The  Anatomy  of  £Mo/)/i/o^/oj.fwm 89 

The  Root  in  Euophioglossum 93 

Anatomy  of  OphtoJerma , 94 

Anatomy  of  Cheiroglossn 99 

The  Sporophyte  of  5o(ry<:/"«m 99 

The  Sporophyte  of  Hclminthost/uhys 104 

The  Sporangiophore  of  the  Ophioglossales 108 

The  Development  of  the  Sporangiophore .        .  1 10 

The  Development  of  the  Sporangium 112 


VI  CONTENTS 

Part  II.   The  Marattiales. 

I.  The  Gametophyte 119-134 

The  ProthaWium  of  KduljnssKi 122 

The  Prothallium  of  Z)rtn<f(i ....  124 

The  Endopliyte  of  the  Marattiaccs 127 

The  Sexual  Organs 128 

The  Antheridium 128 

Spermatogenesis 129 

The  Archegonium 130 

Fertihzation 134 

II.  The  Embryo i35-'59 

The  Embryo  oi  Marattta 136 

The  Embryo  of  Angiopterts ijg 

The  Y.mh\yo  oi  Kauljussia 141 

The  Embryo  of  Z)a««a 142 

The  Anatomy  and  Histology  of  the  Young  Sporophyte 145 

The  Cotyledon    ....                 146 

The  Stem  of  the  Young  Sporophyte 153 

The  Root 155 

The  Second  Leaf               156 

III.  The  Older  Sporophyte 160-208 

The  Development  of  the  Vascular  System  in  Z),;nrSrt 160 

The  Adult  Sporophyte  of  Dtiiura 175 

The  Anatomy  of  the  Leaf 177 

The  Apical  Growth  of  the  Roots 178 

The  Sporophyte  of  Kauljussia i  yg 

The  Sporophyte  of  Marattta 1 88 

The  Adult  Sporophyte  of  A/rtra«(a Ig^ 

The  Sporophyte  of  Angiopterts igj 

The  Adult  Sporophyte  of  Angiopterts 200 

Archangioptcris 203 

Macroglossum 204 

Tissues  of  the  Marattiaceas 204 

The  Sporophyll  of  the  Marattiaceae 204 

The  Sporangium  of  the  Marattiaceae 205 

Part  III. 

The  Origin  and  Relationships  of  the  Eusporangiatae 209 

Conclusion    ...               217 

Bibliography 219 

List  of  Plates 223 

Inde.x 225 


THE  EUSPORANGIATAE 

THE  COMPARATIVE  MORPHOLOGY 

OF 

THE  OPHIOGLOSSACEAE  AND  MARATTIACEAE 


INTRODUCTION. 

It  is  pretty  well  ao;rcf(l  ammio;  botanists  that  most  of  the  seed  plants,  perhaps 
all  of  thcni,  are  dcscemlants  of  some  fern-like  Paleozoic  ancestors.  The  geological 
record  is  remarkably  perfect  in  many  respects,  and  our  knowledge  ofniany  of  these 
Paleozoic  fossils  is  extraordinarily  complete.  Among  the  most  important  con- 
tributions made  of  late  years  to  our  knowledge  of  these  Paleozoic  fossils  is  the  fact 
that  many  of  these  Paleozoic  "ferns"  were  really  seed-bearing  plants  intermediate 
in  character  between  the  true  ferns  and  the  more  highly  develo|)ed  Howering  plants. 

At  best  the  fossil  record  is  very  incomplete  in  regard  to  many  extremely  impor- 
tant structural  details,  and  therefore  it  is  especially  necessary  that  these  points 
should  be  thoroughly  studied  in  such  of  the  existing  ferns  as,  for  any  reason,  seem 
to  be  at  all  closely  related  to  the  ancient  Paleozoic  types. 

The  name  luisporangiane  was  proposed  by  Goebcl  to  include  the  two  very 
peculiar  families  of  fern-like  plants,  the  Marattiaceae  and  Ophioglossacc.x,  which 
differ  in  several  important  respects  from  the  much  more  numerous  and  specialized 
Leptosporangiatac,  the  predominant  ferns  of  the  present  day.  The  Eusporangiatas 
comprise  lOO  or  more  species  of  widely  distributed  ferns,  of  which  the  Marattiaceae 
are  mainly  tropical  in  their  distribution,  while  the  Ophioglossaceae  include  a  good 
many  species  of  temperate  regions  as  well.  The  Kusporangiatae  are  distinguished 
primarily  by  the  character  of  the  sporangium,  which  is  always  much  more  massive 
than  in  the  typical  ferns,  the  Leptosporangiatae.  In  the  latter,  the  sporangium  can 
almost  always  be  traced  back  to  a  single  mother  cell  which  usually  arises  fnim  the 
surface  of  the  leaf,  while  in  the  Eusporangiatse  the  sporangium  is  already  multi- 
cellular when  it  is  first  recognizable. 

The  Marattiaceae  are  in  general  appearance  much  like  the  typical  ferns,  and 
there  is  no  question  of  their  relationship  to  the  Leptosporangiatae.  The  resem- 
blances are  less  obvious  in  the  case  of  the  Ophioglossacea?,  and  some  students  of 
the  ferns  have  expressed  the  opinion  that  the  Ophioglossacea?  should  be  separated 
entirely  from  the  ferns  and  placed  in  a  distinct  class.  (See  Bower  9,)  A  careful 
comparative  study,  however,  of  the  two  families  included  in  the  Eusporangiata'  shows 
so  many  close  correspondences  in  structure,  both  of  the  sporophyte  and  gameto- 
phyte,  that  their  association  together  is  amply  justified. 

The  MarattiaceiP  are  known  to  be  very  ancient  forms,  unmistakable  members 
of  this  family  occurring  abundantly  in  Palet)zoic  formations.  I  he  Ophioglossacea", 
on  the  other  hand,  are  very  unsatisfactorily  represented  in  a  fossil  condition,  and 
for  this  reason  doubt  has  been  thrown  on  their  antiquity,  although  their  structures 
show  strong  evidences  of  an  extremely  primitive  character.  Certain  of  the  oldest- 
known  fossil  ferns,  the  Botryopteridea-,  may  possibly  prove  to  be  relateil  to  the 
Ophioglossacex,  but  the  evidence  at  present  is  not  entirely  conclusive. 

In  spite  of  the  unsatisfactory  nature  of  the  geological  evidence,  I  am  neverthe- 
less strongly  inclined  to  believe  that  the  Ophioglossaceae,  on  the  whole,  represent 
the  most  ancient  type  among  the  living  ferns,  this  conclusion  being  based  upon  a 
very  careful  study  of  the  structure  of  both  gametophyte  and  sporophvte. 

There  are  many  practical  difhculties  in  the  way  of  studying  these  interesting 
ferns,  and  these  difficulties  undoubtedly  account  for  the  comparatively  small  number 
of  researches  that  have  been  made  upon  their  development.  A  few  species,  like 
Ophioglossiiiii  vtilgattnii  and  several  species  of  Butrwh/tnii,  arc  widespread  in  their 


N.  C.  State  CoUego 


^  INTRODUCTION 

range  and  occur  in  the  temperate  regions  of  Europe  and  America;  but  very  much 
the  larger  number  of  these,  including  all  of  the  Marattiace.ne,  are  tropical  or  sub- 
tropical plants  and  are  very  seldom  seen  in  cultivation,  hence  material  for  their 
study  must  be  collected  in  their  natural  habitat. 

The  gametophytes,  or  sexual  plants,  are  seldom  encountered  unless  very 
special  search  is  made  for  them,  and  they  have  been  but  rarely  collected;  and  even 
where  the  spores  can  be  made  to  germinate,  the  long  time  necessary  for  the  growth 
of  the  gametophyte  under  artificial  conditions,  and  the  difficulties  of  rearing  them 
to  maturity,  readily  explain  the  small  number  of  successful  attempts  to  study  these 
plants  under  artificial  conditions. 

As  the  result  of  several  visits  to  the  tropics  of  both  the  Old  and  New  Worlds, 
the  writer  has  collected  material  of  all  of  the  eusporangiate  genera,  except  the 
recently  discovered  Archangiopteris  from  southwestern  China  and  Macroglossiim 
from  Borneo.  It  has  seemed  desirable,  with  this  material  as  a  basis,  to  make  a  some- 
what comprehensive  comparative  study  of  the  whole  group  of  the  Eusporangiatae. 
In  this  study,  especial  attention  will  be  devoted  to  the  structure  and  development  of 
the  gametophyte  and  embryo  and  to  the  development  of  the  young  vegetative  organs 
of  the  sporophyte.  The  general  anatomy  and  histology  of  the  mature  sporophyte 
have  already  been  pretty  satisfactorily  studied  and  described  for  most  of  the  genera 
and  a  particularly  satisfactory  account  of  the  development  of  the  sporangium  has 
been  given  us  in  the  comprehensive  memoirs  of  Professor  Bower  (Bower  5,  6),  and  a 
detailed  investigation  of  these  points  has  hardly  seemed  necessary,  although,  so  far 
as  possible,  the  results  of  the  work  of  previous  investigators  have  been  verified. 

The  writer  has  already  published  various  papers  upon  the  development  of 
both  the  Marattiaceae  and  Ophioglossaceae,  and  these  have  been  freely  drawn  upon 
in  the  preparation  of  the  present  monograph;  but  these  earlier  studies  have  been 
materially  extended  by  further  work  upon  the  species  previously  studied  and  in- 
vestigations have  been  made  upon  a  number  of  species  which  hitherto  have  not 
been  examined  at  all,  or  have  been  studied  only  very  incompletely.  This  is  partic- 
ularly true  of  the  genus  Daneea,  which  has  received  comparatively  little  attention 
hitherto.  An  especially  fine  lot  of  material  of  several  species  of  Daneea  was  col- 
lected in  Jamaica  in  1908  and  an  extended  study  of  the  gametophyte  and  young 
sporophyte  has  been  made,  the  complete  results  of  which  are  now  published  for 
the  first  time.  Attention  has  also  been  given  to  the  development  of  the  young 
sporophyte  in  the  other  eusporangiates,  particularly  in  the  peculiar  genus  Kaul- 
fussia,  which,  like  Daneea,  has  received  less  attention  from  the  students  of  these 
plants  than  have  the  genera  Marattia  and  Angiopteris. 

Of  late  there  has  been  a  tendency,  especially  among  students  of  the  fossil  ferns, 
to  lay  great  stress  upon  the  importance  of  the  structure  of  the  vascular  skeleton  of 
the  ferns  in  the  study  of  their  phylogeny.  It  is  therefore  highly  important  that  a 
careful  examination  should  be  made  of  the  origin  and  development  of  the  vascular 
system  in  those  forms,  i.  e.,  the  Eusporangiatae,  which,  there  is  good  reason  to  sup- 
pose, are  the  nearest  relations  among  living  plants  of  the  ancient  Paleozoic  ferns. 

The  results  of  the  writer's  studies  on  the  development  of  the  fibro-vascular 
bundles  of  the  sporophyte  in  all  of  the  eusporangiate  ferns  have  led  to  some  rather 
unexpected  conclusions  as  to  the  real  nature  of  the  vascular  system  in  these  ferns, 
conclusions  decidedly  at  variance  with  the  views  generally  accepted  at  present. 
These  results  have  seemed  sufficiently  important  to  warrant  a  more  extended  treat- 
ment of  this  subject  than  was  at  first  contemplated;  and  this  will  explain  what 
might  otherwise  seem  to  be  a  disproportionate  amount  of  space  devoted  to  the  origin 
and  development  of  the  fibro-vascular  system  in  the  young  sporophyte. 


PART  1.    THi-:  oi^hio(;lossales. 

IIk'  Ophioglossales,  the  "adder-tongue"  ferns,  include  three  genera  (of  which 
two  arc  practically  cosmopolitan)  and  embrace  numerous  species,  being  sometimes 
further  divided  into  several  subgenera;  the  third  genus  is  a  monotypic  one,  confined 
to  the  tropics  of  the  Old  World.  These  three  genera  are  evidently  (juite  closely 
related  among  themselves  and  may  without  hesitation  be  referred  to  a  single  family, 
the  C)phioglossace;e.  The  genus  Ophioglossum  includes  several  species  of  the 
temperate  regions  of  the  whole  world,  and  some  of  the  species,  like  O.  vulgatum, 
are  very  widespread;  the  tropical  species  are  much  more  numerous,  but  the  number 
of  these  is  very  uncertain  and  much  confusion  exists  as  tt)  the  limits  of  certain  species. 
The  second  genus,  Botrycliiinu,  belongs  mainly  to  the  temperate  regions,  only  a 
small  number  of  species  occurring  in  the  tropics,  and  these  are  principally  confined 
to  the  cooler  mountain  regions.  1  he  third  genus,  Helmmthostnchys,  with  a  single 
described  species,  H.  ze\liiiii\a,  is  a  not  uncommon  fern  of  the  lowland  forests  of 
the  Indo-Malayan  region. 

rhe  Ophioglossacea;  are  for  the  most  part  quite  glabrt)us  plants,  of  small  or 
moderate  size.  The  smallest  species,  like  Botrychium  simplex  and  some  of  the 
smaller  species  of  Ophioglossum  (e.  g.,  0.  californicum,  O.  bergtannm,  and  some  of 
the  smaller  forms  of  O.  nioliicc/iniim)  may  be  only  5  or  6  centimeters  in  height.  The 
largest  species  of  Botrychium  and  Hclminthostachys  sometimes  attain  a  height  of 
50  centimeters  or  more,  with  ample,  much-dissected  leaves,  while  the  long,  ribbon- 
like, pendent  leaves  of  the  epiphytic  Ophioglossum  pendulum,  the  giant  of  the  family, 
may  reach  a  length  of  1.5  meters. 

Except  for  two  species  of  Ophioglossum  belonging  to  the  sections  O phioderma 
and  Cheiroglossa,  the  Ophioglossaceae  are  terrestrial  plants,  usually  growing  in  soil 
abounding  in  humus,  and  the  gametophyte  in  all  cases  is  a  subterranean  structure 
quite  destitute  of  chlorophyll. 

The  stem  is  a  rhizome,  which  is  short  and  upright  in  the  terrestrial  species  t)l 
Ophioglossum  and  in  Botrychium,  but  is  dorsiventral  in  Helminthostachys  and  the 
epiphytic  species  Ophioglossum  pendulum.  In  most  of  the  species  of  the  temperate 
regions  only  a  single  leaf  is  developed  each  year,  but  there  are  some  exceptions  to 
this  rule  in  Ophioglossum,  especially  in  the  tropical  species,  where  there  is  no 
interruption  of  the  growth. 

The  leaves  are  usually  ample,  and  may  be  (juite  undivided,  as  in  most  species 
of  Ophioglossum,  or  they  may  be  dichotomously  divided  in  O.  pnlmnium  and  some 
forms  of  O.  pendulum;  or  they  may  be  much  dissected,  usually  in  a  ternate  fashion, 
in  Botrychium  and  Helminthostachys.  The  sporangia  are  sometimes  very  large, 
and  are  borne  upon  characteristic  spikes,  or  "sporangiophores,"  whose  morpho- 
logical nature  is  a  matter  of  some  controvers\'.  The  venation  of  the  leaves  is 
reticulate  in  all  species  o(  Ophioglossum,  but  in  the  other  genera  ir  resembles  that 
of  the  typical  ferns. 

With  the  exception  of  Ophioglossum  (Cheiroglossa)  palmatuni,  the  sporangio- 
phore  is  normallv  attached  to  the  adaxial  side  of  the  leaf,  usually  near  the  junction 
of  the   laminii   and    prtiole;    but   sometimes  it  is  inserted    much    lower   down,  or  it 


0  THE    OPHIOGLOSSALES 

may  arise  close  to  the  base  of  the  petiole  and  appear  to  be  quite  independent  of 
the  sterile  leaf  segment.  The  sporangia  range  in  number  from  about  half  a  dozen, 
in  some  of  the  smaller  forms  of  Botrychtum  simplex  and  Ophioglossum,  to  many 
hundred  in  such  large  species  as  Botrychium  vtrgtnianiim  and  Helminthostachys. 
There  is  a  most  interesting  series  of  forms  connecting  the  smaller  and  simpler  types 
with  the  large  and  complicated  ones.  With  the  increasing  complexity  of  the  sporan- 
giophores,  there  is  usually  a  reduction  in  the  size  of  the  sporangia,  which,  however, 
become  better  differentiated  than  in  the  simpler  types. 

There  is  no  question  about  the  close  relationships  existing  between  the  dif- 
ferent genera  of  the  Ophioglossaceae,  but  there  is  some  difference  of  opinion  as  to 
their  connection  with  other  Pteridophytes.  While  they  are  probably  sufficiently 
distinct  to  be  relegated  to  a  special  order,  Ophioglossales,  their  peculiarities  hardly 
warrant  separating  them  entirely  from  the  ferns.  As  will  be  seen  later,  they  offer 
many  points  of  resemblance  to  the  Marattiales,  both  in  regard  to  the  structure  of 
the  adult  sporophyte  and  that  of  the  gametophyte  or  sexual  plant,  and  the  early 
phases  of  embryonic  development.  These  resemblances  are  too  numerous  and  too 
exact  to  make  it  at  all  likely  that  the  two  orders  are  unrelated. 

I.  THE  GAMETOPHYTE. 

The  first  discovery  of  the  gametophyte  of  the  Ophioglossaceae  was  made  by 
Hofmeister  (Hofmeister  1)  who,  in  1854,  found  the  gametophyte  of  Botrychium 
liiuaria;  two  years  later  Mettenius  (Mettenius  1)  described  much  more  fully  the 
prothallium  of  Ophioglossum  peduncuhsum,  which  was  cultivated  in  the  botanical 
garden  at  Leipzig.  No  further  additions  were  made  to  the  subject  until  the  writer 
(Campbell  4)  succeeded  in  obtaining  the  first  germinating  stages  of  O.  pendulum, 
collected  in  the  Hawaiian  Islands,  and  those  of  Botrychium  virginiatium;  and  the 
older  gametophyte  of  the  latter  species  was  also  described.  In  the  year  1898  Jeffrey 
(Jeffrey  1)  published  a  complete  account  of  the  gametophyte  and  embryo  of  Bo- 
trychium virgmianum.  Later  contributions  to  the  subject  are  those  of  Lang 
(Lang  I)  on  the  gametophyte  of  Ophioglossum  pendulum  and  o{  Helminthostachys; 
and  the  papers  of  Bruchmann  (Bruchmann  1,  2)  on  the  prothallium  of  Botrychium 
lunaria  and  Ophioglossum  vulgatum.  In  1905,  Lyon  (Lyon  1)  published  a  brief 
account  of  the  embryo  of  Botrychium  ohliquum. 

In  1906  I  collected  in  Ceylon  a  few  prothallia  of  a  species  of  Ophioglossum 
which  may  have  been  O.  reticulatum,  and  shortly  afterward,  during  a  stay  in  Java, 
a  number  of  prothalliaof  O.  moluccanmn  were  found,  as  well  as  a  few  belonging  to 
an  undetermined  species  associated  with  the  latter.  During  my  stay  in  Java  I  was 
fortunate  enough  to  obtain  also  a  large  number  of  prothallia  of  O.  pendulum.  An 
account  of  these  has  already  been  published  (Campbell  8). 

All  species  of  the  Ophioglossaceae  that  have  yet  been  examined  agree  in  the 
underground  habit  and  saprophytic  nature  of  the  gametophyte,  which  always  has 
associated  with  it  a  peculiar  endophytic  fungus,  or  "mycorrhiza,"  which  is  un- 
doubtedly connected  with  the  assimilation  of  organic  food.  Mettenius  states  that 
chlorophyll  may  be  developed  if  the  prothallium  appears  above  ground,  and  Bruch- 
mann found  that  this  was  also  true  in  O.  vulgatum;  but  as  a  rule  the  prothallium 
remains  subterranean  and  quite  destitute  of  chlorophyll. 

The  spores  of  the  Ophioglossaceae  are  always  of  the  tetrahedral  type,  and  when 
ripe  possess  a  moderately  thick  sculptured  outer  membrane,  which  is  usually  colorless 
or  pale  yellow,  so  that  the  masses  of  spores  are  either  white  or  a  pale  sulphur-yellow 
tint.     The  ripe  spore  as  a  rule  is  packed  with  granular  matter,  which  make.s  the 


CAMI-lOl'in  IF 


contents  appf;ii  ()|i;i(|iii-  iiiul  olisi'iiits  mi>ic  or  kss  ihv  i(nii;ill\  |)l;R-ed  nucleus. 
A  marked  e.\ct|ni(>n  to  the  oidinar)  tv|>i-  ot'spdii-  \\;is  ih;ii  Iduiul  in  .m  luuietermined 
species  o(  Opliioglossuin  collected  at  Hiiitenzorg  in  Java.  1  his  was  supposed  to  be 
O.  moliiccfimini,  with  which  it  was  {^rowinj^;,  hut  a  comparison  with  typical  specimens 
of  the  latter  species  showed  marked  tlitterences,  the  most  stiiking  being  the  spores, 
which  were  larger  than  in  the  type,  had  much  less  dense  contents,  and  were  espe- 
cially notable  in  that  they  had  regulaily  two  nuclei,  a  condition  unique,  so  far  as  I 
know,  among  the  ferns.  (See  Campbell  8,  fig.  157.)  The  granular  contents  of  the 
spores  include  numerous  albuminous  granules,  together  with  more  or  less  starch 
and  oil. 

(;krmination  in  oimiioglossum. 

1  he  first  successful  attempts  to  germinate  the  spores  of  Ophioglossiini  were 
made  by  me  in  1892,  when  ripe  spores  of  the  epiphytic  ().  pendulum  were  collected 
in  Hawaii  and  brought  to  California.  1  his  species  was  found  in  Hawaii,  growing 
usually  upon  the  trunks  of  tree  ferns,  and  the  spores  were  sown  upon  bits  of  the 
bark-like  masses  of  roots,  which  in  the  commoner  tree  ferns  of  Hawaii  (species  of 
Cihotiuni)  cover  the  trunk  with  a  thick,  felted  mass.  These  masses  of  roots  were 
kept  in  jars,  and  the  spores  were  sown  upon  them,  a  good  many  of  them  germinating 
in  course  of  time.  Fhe  germination  was  very  slow,  the  spores  often  remaining 
unchanged  for  months,  and  none  of  these  young  prothallia  developed  beyond  the 
stage  with  three  cells.  This  failure  to  develop  further  was  undoubtedly  due  to  the 
fact  that  they  did  not  become  infected  with  the  mycorrhiza,  which  is  essential  to  the 
full  development  of  the  prothallium. 

In  1906  ripe  spores  of  the  same  species  were  collected  in  Ceylon  and  Java. 
In  Ceylon  spores  were  secured  at  the  botanical  garden  in  I'eradeniya  and  in  the 
Barrawa  Reserve  Forest  near  Hanwella,  where  Lang  obtained  his  material.  In  Java 
the  spores  were  mostly  collected  at  Tjibodas.  In  all  of  these  later  experiments  the 
spores  were  sown  in  humus  collected  from  about  the  base  of  the  spore-bearing 
plants.    These  masses  of  wet  humus  were  kept  in  stoppered  bottles. 

As  in  the  earlier  experiments, 
the  germination  was  slow,  the  first 
germinating  stages  being  found  only 
after  a  month  or  more,  and  in  some 
cases  the  spores  remained  un- 
changed for  a  very  long  period.  The 
bottles  containing  -the  spores  sown 
upon  the  humus  were  brought  back 
to  California,  and  a  recent  exami- 
nation (September  1909)  showed  a 
considerable  number  of  apparently 
normal  spores,  as  well  as  living 
three-celled  prothallia,  presumably 
the  result  of  comparatively  recent 
germination. 

Spores  sown  in  Tjibodas  on 
April  18,  1906,  were  first  found 
germinating  at  Buitenzorg  on  May 
24,  germination  at  this  time  being  pretty  well  advanced.  On  June  T,  a  number  of 
these  had  three  cells.  The  germination  (fig.  i )  in  all  cases  coi  responded  closely  with 
the  writer's  former  observations  and  closely  resembles  that  which  we  shall  see  pres- 
ently in  OpIiKiolfissuru  uKilucniiiuiii.     In  no  case  could  any  chloroplull  be  detected. 


(icrmin.iting  spore  of  Ophioglouum  pendulum.   X360. 
Optical  section  of  A. 

Three  views  of  a  very  young  gametophyte  of  0.  pendulum,  showing 
infection  by  mycorrhizal  fungus.     X360. 


8  THE    OPHIOGLOSSALES 

and  apparently  the  prothallium  of  0.  pendulum  is  strictly  saprophytic  throughout 
its  existence. 

The  extremely  favorable  conditions  for  plant  growth  at  Buitenzorg  made  this 
an  unusually  promising  place  for  studying  germination,  and  very  soon  after  my 
arrival  there  a  quantity  of  plants  of  Ophioglossum  moluccaiiutn,  or  what  was  sup- 
posed to  be  this  species,  was  secured,  and  the  spores  were  sown.  Subsequent  study 
showed  that  at  least  three  species  grew  together  at  Buitenzorg,  so  that  it  is  not  at 
all  certain  that  all  of  the  germinating  spores  and  the  prothallia  which  were  col- 
lected later  really  belonged  to  O.  mohiccanum. 

Since  in  all  previous  experiments  with  the  Ophioglossaceae  germination  had 
been  very  slow,  it  was  with  much  surprise  that  the  first  lot  of  spores  that  were  sown, 
when  examined  a  week  later,  were  found  to  be  germinating  very  freely  and  had 
evidently  been  growing  for  some  days.  New  sowings  were  made,  and  in  some  cases 
the  first  germination  stages  were  evident  within  three  days  from  the  time  the  spores 
were  sown.  Inasmuch  as  the  spores  contain  no  chlorophyll,  this  rapid  germina- 
tion is  really  remarkable.  In  the  most  favorable  instances  the  greater  part  of  the 
spores  germinated  and  many  thousand  germinating  spores  were  studied. 

The  first  sowings  were  made  upon  earth  taken  from  where  the  plants  were 
growing;  the  earth  was  placed  in  small  glass  dishes  and  flooded  with  water;  the 
spores  were  then  scattered  over  the  surface  of  the  water,  some  sinking,  but  the 
greater  part  floating  on  the  surface.  In  later  experiments  cavities  were  hollowed 
out  in  the  earth  and  these  were  filled  with  water,  while  the  rest  of  the  earth  was 
left  wet,  but  not  flooded.  It  was  found  that  the  spores  germinated  more  promptly 
in  the  water  than  on  the  wet  earth,  and  this  suggested  that  probably  under  natural 
conditions  germination  occurs  where  the  spores  fall  in  slight  depressions  which  are 
filled  with  water  for  a  time  after  heavy  rains.  The  prothallia  oi Hehninthosiachyi, 
to  judge  from  the  locality  where  they  were  found  in  the  Barrawa  Forest,  occurred 
only  where  the  forest  was  subject  to  inundation,  and  it  may  be  that  immersion  in 
water  is  necessary  for  the  germination  oi  Ophioglossum  moluccanum,  or  at  any  rate 
facilitates  germination.  The  older  prothallia  of  this  species  which  were  found  in 
Buitenzorg  were  growing  in  low  ground  between  the  projecting  roots  of  trees,  where 
water  might  very  well  stand  for  some  days  in  wet  weather. 

The  first  sign  of  germination  consists  in  the  enlargement  of  the  spore  contents, 
which  soon  burst  the  rigid  outer  membrane  along  the  three  lines  upon  its  ventral 
face,  and  through  the  cleft  thus  formed  the  spore  contents,  surrounded  by  the  col- 
orless inner  membrane  ("endospore"  or  "intine")  protrude  as  a  blunt  papilla 
(plate  I,  fig.  2).  The  first  division  wall  is  transverse  and  is  soon  followed  by  a 
second  wall  in  the  upper  cell  (i.  e.,  the  one  turned  away  from  the  opening).  The 
second  wall  is  at  right  angles  to  the  first,  and  the  young  prothallium  now  consists  of 
three  cells,  the  basal  one,  which  is  partly  exposed  through  the  cleft  at  the  upper  side 
of  the  spore,  and  the  two  upper  cells,  which  have  more  dense  contents  than  the 
basal  one.  The  basal  cell  in  position  corresponds  to  the  first  rhizoid  in  the  germi- 
nating spore  of  the  typical  ferns,  but  it  was  never  found  to  become  extended  into  a 
true  rhizoid,  and  no  rhizoids  were  seen  in  any  of  the  very  young  prothallia. 

While  Ophioglossum  moluccanum  and  O.  pendulum  agree  very  closely  in  the 
early  stages  of  germination,  in  the  latter  species  no  trace  of  chlorophyll  can  be 
detected  at  any  time,  but  in  O.  moluccanum  it  is  not  uncommon  to  find  from  one  to 
three  chloroplasts  present.  These  chloroplasts  are  very  pale  in  color,  but  it  is 
certain  that  a  small  amount  of  chlorophyll  is  present  in  some  cases. 

While  most  of  the  young  prothallia  oi  Ophioglossum  moluccanum  do  not  advance 
beyond  a  three-celled  stage,  a  few  were  found  in  which  there  were  four  cells,  but  all 


THr-:  c;ami-toi>hvti-;  y 

attempts  to  cany  tluiii  1)c\()ik1  this  stage  failed  and  after  exhaiistinir  the  spore  con- 
tents they  soon  died.  Ihe  small  amount  of  chlorophyll  (jccasionall)-  found  in  these 
young  prothallia  is  evidently  insufficient  for  their  independent  growth,  and  after  a 
few  weeks  the  granular  contents  all  disappear  and  the  cells  soon  collapse,  showing 
that  the  young  gametophyte  has  died  from  starvation. 

A  number  of  specimens  of  the  rare  Ofiliioglossiun  intcniircltiini  were  collected 
near  IJuitenzorg  and  a  few  ripe  spores  were  also  secured.  I'hese  spores  contain 
somewhat  less  dense  contents  than  those  of  the  other  species  described  and  have  a 
more  delicate  epispore.  Spores  were  sown  on  March  30  in  Buitenzorg,  and  when 
examined  about  two  weeks  later  no  germinations  were  found,  nor  did  a  second 
examination  about  the  end  of  April  show  any  further  results.  On  May  21,  however, 
two  three-celled  prothallia  were  found,  and  subsequently  a  small  number  of  others, 
but  no  later  stages  were  discovered.  The  young  prothallia  appeared  in  every 
respect  like  the  similar  stages  in  the  other  species  (plate  i,  fig.  6). 

In  Ophioglossum  periclulum  a  number  of  young  prothallia  were  found  which 
had  increased  very  much  in  size  and  undergone  further  division.  'Ihe  first  of 
these  were  observed  on  April  3,  and  had  developed  from  spores  sown  in  Peradeniya 
on  February  9.  These  young  prothallia  (fig.  i,  ,)  had  from  four  to  six  cells.  It 
was  found  that  in  each  case  the  mycorrhiza  had  connected  itself  with  the  young 
prothallium,  and  evidently  had  caused  a  stimulus  in  its  growth.  In  every  case 
where  the  young  prothallium  had  more  than  three  cells  there  was  found  associated 
with  it  the  mycorrhiza,  which  could  be  easily  seen  to  penetrate  into  the  basal  cell. 
The  infection  was  in  all  cases  due  to  fragments  of  mycelium,  and  in  no  case  to  any- 
thing which  could  be  interpreted  as  spores.  The  fungus  was  apparently  growing 
free  in  the  humus  where  the  spores  were  sown.  This  soil,  as  we  shall  see,  was  taken 
from  about  the  roots  of  the  sporophytes  which  furnished  the  spores. 

The  free  surface  of  the  basal  cell  has  its  wall  decidedly  thickened,  and  it  was 
here  that  the  infection  took  place  in  all  the  specimens  seen.  The  branching  mycelium 
of  the  mycorrhiza  was  closely  applied  to  the  surface  of  the  cell  and  a  haustorium  was 
sent  down  through  the  cell  wall  into  the  basal  cell  (fig.  i,  m).  This  haustorium  is 
pointed  at  first,  but  after  it  penetrates  into  the  cell  it  enlarges  and  assumes  the  form 
of  a  somewhat  thickened  worm-shaped  body,  much  thicker  than  the  free  mycelium 
outside.  In  the  cell  infected  with  the  fungus,  the  contents  show  the  peculiar  aggre- 
gated appearance  characteristic  of  the  infected  cells  of  the  older  prothallia.  On 
the  6th  of  April  a  specimen  with  seven  cells  was  found.  About  a  month  later,  a 
number  of  other  specimens  were  observed  also,  some  of  these  having  as  many  as 
thirteen  cells  (plate  i,  fig.  9).  This  was  the  largest  number  found  in  any  of  the 
young  prothallia. 

The  divisions  of  these  young  prothallia  are  mainly  in  the  lower  cells,  so  that 
the  apex,  as  in  the  prothallium  of  the  true  ferns,  develops  mainly  from  the  lower  of 
the  two  original  prothallial  cells.  The  basal  cell,  however,  al.so  undergoes  divisions, 
and  there  is  no  very  marked  difference  between  the  lower  and  upper  ends  of  the 
prothallium.  At  this  stage  there  is  a  marked  resemblance,  except  for  the  absence 
of  chlorophyll,  to  the  early  germination  stages  o(  Lvropocliiini  ceriniinu  (Treub  I). 
The  mycorrhiza  penetrates  the  cells  adjacent  to  the  one  first  infected,  but  leaves  the 
apical  region  free,  and  this  region  probably  remains  permanently  free  from  the 
endophyte,   as  it  does  in  the  adult  prothallium. 

'ihe  number  of  young  prothallia  found  was  too  small  to  make  it  possible  to 
determine  exactly  what  may  be  considered  to  be  the  normal  succession  of  cell  divi- 
sion, and  whether  at  this  early  stage  there  is  a  definite  apical  cell  could  not  In-  decicUd. 
As  will  be  seen  from  the  figures,  there  is  evidently  a  good  deal  of  variation  in  the 


10  THE    OPHIOGLOSSALES 

early  divisions.  In  these  larger  prothallia  there  is  already  the  beginning  of  an  axial 
tissue.  Whether  the  cell  v  (plate  i,  fig  q)  is  to  be  regarded  as  an  apical  cell,  it  would 
be  hard  to  say. 

Owing  to  my  departure  from  |ava  about  three  months  after  the  first  observa- 
tions were  made,  it  was  impossible  to  trace  the  development  of  the  prothallia  further, 
but  this  much  is  certain — without  the  infection  of  the  fungus,  growth  will  not  pro- 
ceed beyond  the  three-celled  stage,  and  apparently  in  0.  pendulum  no  chlorophyll 
will  develop  under  any  conditions,  and  the  prothallium  from  its  earliest  stages  must 
be  considered  saprophytic  in  its  nutrition.  Whether  the  oval  body  described  as  the 
product  of  germination  is  to  be  considered  as  a  sort  of  tubercle,  such  as  is  found  in 
Lycopodium  cernuum,  must  be  decided  by  further  investigations.  Lang's  descrip- 
tions and  figures  of  the  smallest  specimens  which  he  discovered  would  indicate 
that  this  is  not  the  case  in  0.  pendulum;  but  the  tuberous  body  usually  found  at  the 
base  of  the  older  prothallia  in  0.  moluccauuni  (and  this  is  true  also  in  O.  vulgatum) 
would  indicate  that  in  these  species  it  is  not  impossible  that  a  primary  tubercle 
is  first  formed  and  subsequently  the  fertile  branch. 

THE  ADULT  GAMETOPHYTE  OF  OPHIOGLOSSUM. 

In  1856  Mettenius  (Mettenius  1)  found  the  gametophyte  of  O.  pedunculosum 
Desv.,  a  tropical  species,  growing  spontaneously  in  the  pots  where  the  plants  had 
been  cultivated  in  the  botanical  garden  at  Leipzig.  He  did  not  succeed,  however, 
in  making  the  spores  germinate.  These  prothallia  were  slender,  subterranean 
bodies,  sometimes  branched,  sometimes  without  branches.  They  ranged  in  length 
from  1.5  lines  to  2  inches  (fig.  3,  A,  B).  There  was  usually  present  a  basal  enlarge- 
ment or  tuber,  from  which  the  fertile  part  of  the  prothallium  extended.  The  older 
portions  were  brownish  in  color;  the  growing  tips  of  the  branch  white.  From  the 
surface  there  grew  numerous  short  brown  rhizoids.  Archegonia  and  antheridia 
grew  more  or  less  intermingled  and  were  formed  in  large  numbers.  Except  for  the 
greater  size,  these  prothallia  closely  resemble  those  of  O.  moluccanum  collected  by 
me  in  Buitenzorg;  and  as  O.  pedunculosum  Desv.  has  been  held  to  be  a  synonym 
of  O.  moluccaniim-^chXtcht,  it  is  possible  that  Mettenius's  plants  were  the  same  as 
those  found  by  me  growing  in  Buitenzorg  in  Java.* 

The  next  account  of  the  prothallium  oi  Opliioglossum  is  that  of  Lang  (Lang  1). 
He  collected  in  Ceylon  specimens  of  the  prothallia  of  Opliioglossum  pendulum. 
These  were  found  in  the  Barrawa  Reserve  Forest,  not  far  from  Colombo,  and  were 
buried  in  the  humus  accumulated  between  the  leaf  bases  oi  Poly  podium  quercifolium, 
an  epiphytic  fern  to  which  O.  pendulum  is  often  attached.  I  visited  this  same  locality 
in  February,  1906,  but  was  unsuccessful  in  collecting  the  prothallia,  although  I 
obtained  numbers  of  the  sporophytes.  Some  time  after,  however,  when  in  Java,  I 
found  a  very  large  number  of  prothallia  which  were  growing  in  much  the  same  way 
as  those  collected  by  Lang,  except  that  in  this  case  the  fern  to  which  the  Ophio- 
glossum  was  attached  was  the  widespread  bird's-nest  fern,  Asplenium  nidus. 

Bruchmann  has  given  a  detailed  account  of  the  prothallium  of  the  widespread 
O.  vulgatum,  which  agrees  closely  in  its  essential  details  with  0.  pedunculosum  and 
O.  moluccanum.  Bruchmann's  specimens  were  collected  in  the  Thuringian  Forest, 
in  a  depression  that  w*as  subjected  at  times  to  overflow,  a  condition  paralleled  by  the 
locations  where  the  prothallia  of  Helminthostachys  were  collected  by  Lang  and 

*  Cristensen  in  his  recent  Index  Filicum  (1906)  regards  0.  moluccanum  as  a  synonym  of  0. pedunculosum.  Through  the  kind- 
ness of  Professor  K.  Goebel,  I  recently  had  an  opportunity  of  examining  some  specimens  of  O.  pedunculosum  growing  in  the 
botanical  garden  in  Munich.  These  plants  were  the  descendants  of  the  specimens  in  Leipzig  described  by  Mettenius  and  certainly 
very  closely  resembled  the  typical  O.  moluccanum  from  Buitenzorg. 


THE    GAMF.TOPHYTK  11 

mysfir,  ;in(l  ;il.s(i  liki-  the  l()calit\'  wlun-  inosr  of  my  s|Hi.iiiun.s  of  (J.  tnoliimniiirn 
were  iouiul  in  |ava.  1  liis,  in  (.onnection  uitli  my  expLiimciits  in  gciininating  the 
spores  of  O.  nwliKcamitti,  makes  it  not  unlikely  that  actual  submersion  is  a  necessary 
condition  for  the  germination  in  the  terrestrial  species  ot  Ophio^losstitn. 

In  April  1906,  about  fifty  prothallia  of  O.  nioluccanuni  were  collected  by  me 
at  Buiten/org,  where,  as  we  have  seen,  this  species  is  extremely  abundant.  Only  a 
small  number  of  these  were  young  enough  to  show  the  young  reproductive  organs, 
and  most  of  them  had  already  developed  the  young  sporophyte.  The  greater  part 
of  these  prothallia  were  found  growing  together  in  a  slight  depression  between  the 
projecting  roots  of  a  tree. 

These  prothallia  were  slender  bodies,  from  5  to  10  millimeters  in  length,  and  none 
of  them  branched.  They  showed  a  more  or  less  conspicuous  basal  tuber,  like  that 
described  by  Mettenius  for  O.  peJunculosum,  and  indeed  they  very  closely  resembled 
his  figures  of  the  simpler  forms  of  that  species,  but  are  very  much  smaller.  The 
youngest  specimen  found  (plate  i,  fig.  10)  consisted  of  a  small,  irregular  tuberous 
body  of  a  brownish  color,  from  which  grew  a  short  appendage  or  branch,  the  tip  of 
which  was  white.  The  older  ones  also  showed  this  basal  tuber,  but  the  cylindrical 
branch  was  much  longer.  Owing  to  their  slender  form,  the  prothallia  are  not  always 
easily  distinguishable  from  roots,  and  in  some  cases  a  microscopic  examination  is 
necessary  before  one  can  be  sure  of  their  real  nature.  Growing  from  the  surface  are 
scattered  short  brown  hairs  like  those  described  by  Mettenius  for  0.  peJunculosum. 
Archegonia  and  antheridia  are  formed  at  an  early  period,  and  can  be  traced  to  the 
base  of  the  fertile  branch,  or  in  some  cases  may  be  found  even  upon  the  tuber.  In 
these  specimens  the  reproductive  organs  seemed  to  be  formed  in  rather  smaller 
numbers  than  is  the  case  either  in  0.  pednnciilosum  or  O.  vulgatum.  Among  the 
prothallia  was  one  very  much  larger  than  the  others  which  had  very  large  numbers 
of  old  archegonia.  It  is  highly  probable  that  this  represents  a  second  species,  but 
unfortunately  there  was  no  means  of  determining  to  which  of  the  two  or  three 
forms  associated  under  the  name  0.  moluccmnnn  it  belonged. 

The  cells  of  the  tuber  and  the  lower  part  of  the  branch  contain  the  character- 
istic endophytic  fungus,  but  the  greater  part  of  the  fertile  branch  is  quite  free  from 
this,  and  the  cells  appear  almost  transparent,  but  they  contain  numerous  small  starch 
granules.  The  endophyte  is  much  more  abundant  in  the  cells  of  the  tuber.  The 
hyphre,  which  stain  readily  with  gentian  violet,  are  irregular  in  outline  and  branch 
freely.    Very  often  branches  can  be  seen  piercing  the  walls  of  adjacent  cells. 

In  the  living  condition  the  pointed  apex  of  the  prothallium  is  pure  white,  and 
even  with  a  hand  lens  the  projection  of  the  antheridia  is  clearly  evident.  Mettenius 
noticed  this  "varicose"'  appearance  t)f  the  smaller  prothallia  in  0.  pedunculosuvi. 
A  median  section  of  the  branch  shows  that  the  end  is  decidedly  pointed  and  has  a 
clearly  defined  apical  cell.  Owing  to  the  very  small  amount  of  material  available, 
no  satisfactory  transverse  section  of  the  apex  could  be  made,  and  it  can  not  be  told 
whether  the  apical  cell  in  transverse  section  is  three-sided,  as  described  by  Hruch- 
mann  for  O.  vulgatum,  or  is  four-sided,  as  it  is  in  O.  pendulum.  In  the  smaller  speci- 
mens antheridia  were  more  numerous  than  archegonia,  although  several  of  the  latter 
were  present.  The  antheridia  arise,  in  general,  in  acropetal  succession,  but  it  is 
not  unlikely  that  secondary  ones  may  be  formed  also.  The  archegonia  are  scattered 
among  the  antheridia  apparently  without  anv  definite  order.  In  some  specimens, 
especially  in  the  larger  ones,  the  old  archegonia  were  found  in  great  numbers,  many 
more  than  the  antheridia.  In  other  specimens  a  considerable  part  of  the  protliallium 
was  (juiie  destitute  of  either  archegonia  01  antlu  1  iilia,  and  in  this  respect  the  pro- 
fhalluini  <il   O.  moliiccauum  differs   fioni   that  ot    ().  f^eduih  uh^sum  or  O.  vulgatum. 


12 


THE    OPHIOGLOSSALES 


The  gametophyte  of  ().  moluccaiiiun  shows  a  greatei  or  less  miinber  of  rhizoids 
both  at  the  base  and  along  the  fertile  branch  (plate  i,  fig.  lo).  In  the  more  slender 
forms,  however,  these  rhizoids  are  few.  They  are  in  some  cases  two-celled,  but  more 
commonly  consist  of  a  single  elongated  cell.  It  is  not  unusual  to  find  within  this  the 
penetrating  filament  of  the  mycorrhiza,  as  has  been  described  for  other  species 
of  Ophioglossiim.  The  rhizoids  are  much  longer  relatively  than  in  O.  pciididum. 
According  to  Bruchmann,  the  rhizoids  are  quite  absent  from  the  prothallia  of  O. 
vulgatum. 

Mettenius  states  that  in  O.  pcduncidosum  the  prothallia  often  appear  above  the 
surface  of  the  earth,  and  they  then  become  somewhat  flattened  and  sometimes 
divided  into  several  small  lobes,  and  in  such  cases  chlorophyll  is  developed.  Met- 
tenius, however,  does  not  note  any  further  development  of  these  green  lobes. 
Bruchmann  found  that  chlorophyll  might  also  develop  in  0.  vulgatum,  when  the 
prothallia  were  exposed  to  the  light,  but  he  did  not  find  any  flattening  of  the  apex. 
Owing  to  the  very  small  number  of  growing  prothallia  found  by  me,  I  could  not 
test  the  power  of  developing  chlorophyll  in  0.  mohiccanum,  but  the  occurrence  of 
chromatophores  in  the  germinating  spores  makes  it  highly  probable  that  chlorophyll 
may  be  developed  in  the  older  prothallia  under  the  stimulus  of  light. 


Gametophytes,  /ir,  and  young  sporophytes  of  Ophioglossiim  mo/i/rranum  and  allied  species,  slightly  enlarged.  C  and  F  from 
Hakgala,  Ceylon;  the  others  from  Buitenzorg,  Java;  ky  bud  on  primary  root;  /,  primary  leaf;  /",  secondary  leaf;  /,  tuberous 
enlargement  at  base  of  gametophyte. 

The  small  size  of  the  prothallium  in  O.  r?ioluccanum  and  the  cessation  of  growth 
after  the  sporophyte  is  formed  indicate  that  the  gametophyte  lives  only  for  one 
season,  and  this  is  probably  the  case  also  in  Helminthostachys.  In  this  respect 
O.  moluccanum  and  its  allies  differ  markedly  from  O.  pendulum  and  0.  vulgatum, 
where  the  gametophyte  lives  for  many  years. 

At  Hakgala,  in  Ceylon,  an  undetermined  species  of  Ophioglossum  of  the  type 
of  O.  reticulatum  is  common.  After  careful  search,  a  few  prothallia  which  closely 
resembled  those  of  O.  mohiccanum  were  collected  (fig.  i,  C,  F).  The  material  was 
too  scanty  to  make  a  detailed  study  possible,  but  from  the  external  appearance  it  is 
likely  that  the  structural  details  would  closely  resemble  those  of  0.  mohiccanum. 

The  prothallium  of  Ophioglossum  vulgatum,  according  to  Bruchmann  (Bruch- 
mann I),  closely  resembles  that  of  O.  mohiccanum,  but  is  very  much  larger,  some- 
times  reaching  a  length  of  6  centimeters,   and   it  is    not    infrequently  branched 


13 


Fig. 3. 
A,  B.  Gametophytcs  of  Ophioglossum  peduncutosum  (after  Mettcnius). 
C,  D.  Gametophytcs  of  0.  vulgatum  (after  Bruchmann). 
E-G.  Gametophytcs  of  0.  pendulum,    sp,  young  sporophytc;   r,  secondary  root. 


(Hg  -5.  <".').  Iluic  is  .1  mou-  or  less  ci)iis|Mcii(iiis  l);is;il  nilKi,  like  tli;it  Inuiul  in 
O.nioluranuiin,  ami  t'lom  iliis  extends  a  braiuli  iKaiint;  tlit-  iciMocliictivc 
but,  unlike  the  piothal- 
liuni  of  0.  riiohiccaniini, 
there  seems  to  be  a 
complete  absence  of 
ihizoids.  In  general, 
the  form  is  mt)re  irreg- 
ular than  that  of  O. 
itioluicaiium  and  more- 
over it  is  very  long- 
lived.  The  branches 
may  become  detached 
and  thus  form  new  in- 
dividuals. From  the 
rate  of  growth  in  speci- 
mens kept  under  ob- 
servation for  several 
months,  Bruchmann 
concluded  that  they 
might  live  for  twenty  years  or  more.  Where  the  apical  growth  of  a  branch  is 
interfered  with,  there  may  be  a  formation  of  adventitious  buds,  a  phenomenon 
which  is  also  common  in  0.  pendulum. 

Ophioglossum  {Ophwderma)  pendulum,  a  remarkable  epiphytic  species  wide- 
spread through  the  tropics  of  the  Old  World  and  reaching  to  Hawaii,  is  the  giant 
of  the  order,  the  pendent  ribbon-shaped  leaves  sometimes  attaining  a  length  of 
1.5  meters.  The  sporophyte  grows  rooted  in  masses  of  humus,  either  upon  the 
rough  trunk  of  a  tree  fern  or  palm,  or  hanging  from  the  mass  of  humus  accumu- 
lated about  the  base  of  certain  epiphytic  ferns.  The  hivd's-nest  fern.  As plenium 
nidus,  furnishes  the  favorite  substratum  for  this  species  in  the  forest  of  Tjibodas  in 
Java,  where  my  material  was  collected. 

The  young  prothallium  in  0.  pendulum  is  an  ovoid  bod\',  the  somewhat  smaller 
forward  portion  corresponding  to  the  fertile  branch  in  O.  moluccanum  (see  Lang  I, 
page  25).  The  older  ones  become  very  much  larger  than  in  any  other  species  that 
has  been  described,  and  they  branch  freely  in  all  directions,  except  as  their  growth 
is  controlled  by  their  position.  They  are  always  found  buried  in  a  mass  of  humus 
between  the  imbricated  leaf  bases  of  the  fern,  and  are  often  much  flattened  by  the 
pressure  of  the  leaves  between  which  they  are  confined.  Branches  extend  in  all 
directions,  but  their  growth  is  to  some  extent  controlled  by  the  inclosing  leaf  bases 
and  also  by  the  tangled  mass  of  roots  ot  the  fern,  which  grow  in  all  directions  through 
the  mass  of  humus  and  among  which  the  branches  of  the  prothallium  of  the  Opliio- 
glossum  extend.  In  one  instance  several  hundred  were  collected  from  one  large 
plant  of  Jsplennirn  nidus.  The  prothallia  closely  resemble  Lang's  figures  and 
descriptions,  but  in  many  cases  are  very  much  larger  and  more  extensively  branched 
tlian  :in\  of  the  specimens  collected  by  him  in  Ceylon  (plate  i,  figs.  11-14).  The 
largi  r  prothallia  may  be  stellate  in  form,  but  they  are  usually  very  irregular.  The 
branches  penetrate  in  all  directions  between  the  dense  tangle  of  roots  which  the 
Asplenium  sends  into  the  humus  between  its  persistent  leaf  bases,  and  on  pulling 
these  back  a  mass  of  fine  hunuis  is  found,  held  together  by  the  mat  of  roots  so  that 
it  can  be  removed  intact.  Tlu-  protliallia  aie  excessively  brittle,  and  it  is  practically 
impossible  to  remove  tiie  larger  ones  without  a  loss  of  some  of  the  numerous  branches. 


14 


THE    OPHIOGLOSSALES 


These  break  oft  at  the  least  touch,  ami  no  tloubt  serve  to  propagate  the  ganietophyte, 
which  is  apparently  capable  of  unlimited  growth  in  this  way.  It  is  often  impossible 
to  say  whether  the  smaller  gametophytes  that  are  found  loose  in  the  humus  are 
anything  more  than  branches  which  have  become  spontaneously  separated  from 
the  larger  prothallia. 

The  older  parts  of  the  gametophyte  are  dark  brown  in  color,  but  the  tips  of  the 
branches  are  white,  as  in  the  other  species.  The  branching,  as  we  have  seen,  may 
be  very  irregular,  and  old  fragments  kept  moist  often  send  out  great  numbers  of 
adventitious  buds  (plate  i,  fig.  ii)  which  apparently  in  time  develop  into  normal 
prothallia.  A  number  of  the  commoner  forms  are  shown  in  the  figures.  Plate  i, 
fig.  14,  represents  the  largest  one  met  with.     This  is  by  no  means  complete,  as  a 


A.  Longitudinal  section  of  apes  of  gametophyte 

ftrij  two-celled  embryo. 

B.  Apex  more  highly  magnified,  showing  apical  cell,  x. 

C.  Transverse  section  of  a  branch  of  the  gametophyte  of  Ophi 

D.  Apical  cell  of  same. 

E.  F.  short  hairs  from  gametophyte  of  0.  pendulum;  in  E  m; 


iglossum  pendulum. 

y  be  seen  the  endophytic  fungus  fila 


number  of  branches  were  unavoidably  broken  off^  in  removing  it  from  among  the 
tangle  of  roots  in  which  it  was  embedded.  This  specimen  measured  about  15 
millimeters  in  diameter — more  than  twice  the  size  of  the  largest  specimen  secured  by 
Lang.  The  surface  of  the  older  parts  of  the  prothallium  shows  a  slightly  roughened 
appearance  due  to  the  numerous  very  short  papillate  hairs  which  occur  upon 
it.  These  are  never  of  the  slender  form  found  in  0.  moliiccanum  and  perhaps 
are  not  properly  to  be  considered  as  rhizoids.  Dotted  over  the  surface  are  pale 
brown  spots,  easily  seen  with  the  naked  eye,  and  these  on  examination  are  found  to 
be  the  large,  empty  antheridia.  The  branching  is  sometimes  dichotomous,  but 
lateral  branches  may  arise  at  almost  any  point,  and  old  fragments  of  the  prothallia, 
as  already  indicated,  often  develop  many  adventitious  buds,  a  condition  of  things 
which  apparently  obtains  also  in  the  long-lived  prothallia  of  0.  vidgatum.  The 
rate  of  growth  of  prothallia  kept  by  the  writer  for  more  than  a  year,  as  well  as  their 


THK    GAMKTOPHYTI' 


15 


position  in  rlu'  lunnns  alioiit  the  pl.mt,  wluu  iluy  .iii'  louml  in  tin-  nldtr  parts 
between  ie.ivcs  which  nnist  ii.nc  hccn  tliaii  lor  man)' ytais,  imlii.ite  that  they  are 
veiy  long-livcti  anti,  as  we  iiave  seen,  hy  the  leady  sejjaiation  of  tlie  blanches  they 
aie  easily  piopagated. 

THK  IIISIOI.OGY  Ol-  THI-;  OAMICI'OI'HYTE. 

The  younger  portions  of  the  growing  branches  aie  composed  of  thin-walled, 
colorless  parenchyma,  whose  cells  have  a  conspicuous  nucleus,  and  usually  numerous 
small  starch  granules.  In  the  older  portions  ot  the  gametophyte  the  tissue  becomes 
infected  with  the  often-described  endophytic  fungus.  Practically  all  of  the  cells  of 
the  basal  tuber  arc  thus  infested,  but  in  the  fertile  branches  the  cential  tissue  is 
usually  free  fiom  the  fungus,  and  this  mcdulla-likc  central  tissue  is  surrounded  by  a 
more  or  less  definite  mantle  of  cells,  in  which  the  endophyte  is  especially  luxuri- 
ant. The  outermost  cells  ate  piactically  free  fiom  fungus,  although  new  infections 
probably  may  take  place  there  through  these  outer  cells.  In  O.  moluccaniim  the 
endophyte  is  much  less  developed  than  in  O.  pendulum,  this  no  doubt  being  corre- 
lated with  the  much  briefer  duration  of  the  gametophyte  in  the  former  species. 
According  to  Bruchmann,  the  endophyte  is  strongly  developed  also  in  O.  vulgatum. 
Ihe  endophyte,  as  in  the  other  forms  that  have  been  studied,  is  quite  absent  from  the 
apical  region  of  the  branches.  The  limits  of  the  infested  zone  are  not  very  clearly 
marked  and  any  cell  of  the  older  tissue  of  the  gametophyte  may  harbor  the  fungus. 


Fig.  5. 

A.  Longitudinal  section  of  gametophyte  apei  of  0 phiofloaur 

B.  Transverse  section  of  gametophyte  apex,    a,  the  apical  co 

C.  Archegonium.    X225. 

0.  Two  free  spcrmato/oids.    X550.  (All  figures  after  Bruchii 


The  apical  cell  in  O.  pendulutu  is  usually  a  four-sided  pyramid,  and  not  tetra- 
hedral,  as  it  is  in  0.  vulgatum.  In  longitudinal  section  (fig.  4,  D),  the  apical  cell 
appears  triangular  with  a  fairly  regular  segmentation,  but  there  is  also  active  division 
in  the  adjacent  tissue  and  apparently  the  segmentation  of  the  apical  cell  is  not  very 
rapid.  Cross-sections  show  the  apical  cell  to  be  approximately  four-sided  (fig.  16,  //), 
but  the  sides  are  not  always  of  equal  length  and  .sometimes  it  is  almost  triangular  in 
outline;  possibly  it  may  be  that  in  some  cases,  as  in  0.  vulgatum,  it  is  tetrahedral. 
There  seems  to  be  no  absolute  rule,  however,  as  to  the  succession  of  divisions  in  the 
young  segments.  A  inore  or  less  definite  superficial  layer  arises  from  the  first 
periclinal  divisions,  but  anticlinals  follow  rapidly. 


16 


THE    OPHlOGLOSSALli.S 


II IK  GAMETOPHYTE  OF  BOTIO'CIIIUM. 

Hofmeister  (Hofmeister  I),  in  his  studies  of  the  Archcgoniates,  has  included 
Botrychiiim  huiaria,  whose  prothaHium  he  discovered  in  1854.  No  further  contri- 
butions to  our  knowledge  of  the  subject  are  recorded  until  1893,  when  the  writer  dis- 
covered at  Grosse  He,  Michigan,  a  number  of  old  prothallia  of  5.  virgin! an  tim,  with 
the  young  sporophytes  attached.  The  earliest  germination  stages  of  this  species 
were  also  secured.  In  1895,  Prof.  E.  C.  Jeffrey  collected  at  several  points  in  Canada 
a  large  number  of  prothallia  of  this  species,  and  his  account  (Jeffrey  I)  is  much  the 
most  satisfactory  one  which  had  appeared  up  to  that  time.  In  the  spring  of  1903 
Lyon  (Lyon  1)  discovered  prothallia  of  5.  ohliqiiitm  in  Minnesota,  and  the  following 
year  secured  a  few  specimens  oi B.  simplex  and  B.  matricaricEfolium,  but  he  has  only 
published  a  brief  note  in  regard  to  these  species.  He  states  that  the  reproductive 
organs  in  B.  obliquuni  "differ  essentially  from  those  oi  B.  virgin  i  an  inn,"  but  he  does 
not  explain  in  what  these  differences  consist.  Bruchmann,  v^'ho  has  added  so  much 
to  our  knowledge  of  the  gametophyte  of  the  European  Lycopodiaceae  and  Ophio- 
glossaceae,  has  recently  given  a  very  satisfactory  account  of  the  prothallium  and 
embryo  of  B.  lun aria,  which  he(found  in  various  parts  of  Germany  and  Switzerland. 
He  corrected  certain  errors  made  by  Hofmeister  in  his  account  of  the  same  species. 
(Bruchmann  2.) 


i^^M' 


A,  B.  Germinating  spore  (B,  optical  section). 

C.  Three  gametophytes,  X3;  em,  embryo. 

D.  Section  of  gametophyte,  X12;  the  shaded  region  is  that  occupied  by  the  endophyte.      6  antheridia. 

E.  Apical  region  of  gametophyte,  X150. 

F.  short  multicellular  hair  or  paraphysis. 

Owing  to  the.  kindness  of  Professor  Jeffrey,  a  large  number  of  prothallia  and 
young  sporophytes  of  B.  virginianum,  together  with  several  slides  showing  the  se.xual 
organs  and  embryos,  were  put  at  my  disposal.  This  has  made  it  possible  for  me  to 
make  a  very  satisfactory  study  of  the  reproductive  organs  and  embryo  in  this  species. 

The  spores  of  Botrychiiim,  like  those  of  Ophtoglossum,  are  of  the  tetrahedral 
type  and  are  quite  colorless,  their  contents  showing  the  usual  granular  appearance, 
but  without  any  trace  of  chlorophyll.  The  early  stages  of  germination  are  exactly 
like  those  of  Opiiioglossiim,  the  first  division  wall  being  transverse,  this  being  then 
followed  by  a  second  wall  in  the  inner  cell  at  right  angles  to  the  primary  wall  (fig.  6, 
A,  B).  A  few  chloroplasts  were  seen  in  some  of  the  cells,  but  this  does  not  seem  to 
be  a  constant  character  and  perhaps  was  an  abnormality  due  to  the  spores  having 


AMI 


17 


fji-miin.itnl  in  tin  li!:lit.  UiiKlim.inn  i  Im  lulimiinn  2.  p;i<;c  207)  also  found  the 
earliest  stages  in  11.' Iiiii.nia,  ami  these  oHus|).m(led  rxaetly  to  those  in  B.  vir- 
giniamim. 

The  gamet(ii)h\te  of" /^  I'lri^inininnn  is  a  large,  tiiher-like  ho(l\-,  which  grows 
at  a  depth  of  ahoiit  10  centimeters  below  the  surface  of  the  earth.  The  smallest 
of  the  specimens  found  by  Jeffrey  were  2  millimeters  in  length  by  1.5  millimeters 
in  breadth,  exceeding  in  size  the  fully  developed  prothallia  of  li.  liinaria.  The 
older  ones  may  reach  a  length  of  20  millimeters.  The  young  prothallia  are 
quite   smoothly  oval   in  outline  (Hg.  6,  C),  while  the  older  ones  are  more  or  less 


A,  YounR  sporophytc  of  Botrychium   vir 

mum  attached  to  gametophytc,  pr, 

B.  A  pamctophytc  with  small  sporophyte. 


A.  Two  young  gamctophytcs. 

B.  An  older  one,  with   sporophyte,  sp,  attached 

X16. 

C.  Surface  view  of  two  antheridia,  showing  opcrcu' 

lar  cells  (shaded).    X  lOO. 

D.  A  spcrmatozoid.    X500. 


iire^iihn,  ami  oceasiomillv  the  anterior  end  is  divided  into  two  equa' 
|iinl)al)l\-  as  a  lesuli  of  dichotomy.  .'\s  in  Ophioglossitm,  the  older  parr.' 
gametophyte  are  brownish  in  color,  while  the  young  apex  appears  white, 
earlier  stages  they  are  covered  with  numerous  rhizoids,  which  disappear 
less  completely  as  the  prothallium  becomes  older.  The  forward  end  is 
pointed  and  there  is  a  definite  growing  point.  The  antheridia  make  their 
ance  first,  and  together  with  the  archegonia  are  formed  only  upon  the  upper 
of  the  dorsiventral  thallus,  which  is  noticeably  different  in  form  from  the  cyl 
radially  constructed  prothallium  of  Ophioglossiim. 
2 


1  lobes, 
i  of  the 
In  their 
more  or 
slightly 
a  p  pear- 
surface 


18  THE    OPHIOGLOSSALES 

The  antheridia  form  a  more  or  less  evident  row,  even  in  the  very  young 
prothallium,  and  later  this  median  row  of  antheridia  is  raised  upon  an  elevated 
ridge,  upon  whose  sides  the  archegonia  later  make  their  appearance  (fig.  6,  D). 

The  gametophyte  of  B.  lunaria  closely  resemhles  the  early  stages  of  B.  virgin- 
ianum.  It  is  very  much  smaller  and  rarely  exceeds  a  length  of  2  millimeters,  and, 
like  the  young  stages  in  B.  virginimium,  it  is  covered  with  many  long  rhizoids 
(fig.  8,  A,  B.)  The  smaller  prothallia  are  globular  or  oval  in  shape;  the  larger  ones 
somewhat  heart-shaped.  Hofmeister  states  that  the  antheridia  occur  upon  the  upper 
surface  and  the  archegonia  below;  but  Bruchmann  found  that  both  archegonia  and 
antheridia  were  confined  to  the  upper  surface,  as  in  B.  virginianum.  As  in  the 
latter,  also,  the  dorsal  ridge  is  present,  bearing  the  antheridia  upon  its  crest  and  the 
archegonia  upon  its  flanks. 

The  large  prothallia  of  5.  virginianum  live  for  many  years,  and  Jeffrey  even 
found  a  plant  bearing  spores,  which  was  still  connected  with  a  prothallium.  It  is 
probable  that  the  very  much  smaller  prothallia  of  5.  lunaria  have  a  shorter  duration, 
but  in  this  species  also  the  prothallium  persists  for  some  time  after  the  young 
sporophyte  is  established. 

THE  HISTOLOGY  OF  THE  GAMETOPHYTE  OF  BOTRYCHIUM. 

In  B.  virginianum  the  forward  part  of  the  prothallium  is  made  up  of  colorless 
tissue,  which  extends  for  some  distance  beyond  the  youngest  antheridia.  The  apical 
meristem  in  this  species  (fig.  6,  E)  lies  on  the  upper  side  of  the  prothallium;  in  a 
vertical  longitudinal  section  it  shows  a  group  of  columnar  cells,  one  of  which  is 


ion  of  a  gametophyte  of  Ophioglo. 
endopfiytic  fungus.     X20.    The  shaded  region 
Endophyte  from  prothaUium  of  Bolrychium  virgin 
Sporangium-like  enlargements  of  endophyte. 


m  fcnihil 


probably  the  apical  cell;  but  this  is  not  absolutely  certain.  In  B.  lunaria  (see 
Bruchmann  2,  page  209)  the  apical  meristem  occupies  the  middle  region  ot  the 
anterior  surface  of  the  prothallium,  and  is  of  very  limited  extent.  As  in  B.  vir- 
ginianum, its  cells  appear  columnar  in  form,  but  neither  in  longitudinal  section  nor 
in  a  surface  view  could  a  single  initial  cell  be  recognized. 

The  rhizoids  in  B.  virginianum  are  from  i  to  4  millimeters  in  length  and  may 
be  multicellular,  especially  those  which  arise  from  the  crest  and  flanks  of  the  pro- 
thallium, while  those  which  originate  from  the  base  are  unicellular  and  longer  than 
these  multicellular  ones.  It  is  not  unlikely  that  these  multicellular  structures  are 
rather  of  the  nature  of  paraphyses  than  true  rhizoids.  In  B.  lunaria  the  rhizoids 
seem  to  be,  usually  at  least,  unicellular.  In  both  species  the  rhizoids  soon  turn 
brown  and  their  walls  become  strongly  cutinized.     Both  Jeffrey  and  Bruchmann 


THE    GAMETOI'HYTK  19 

observed  the  penetration  of  fungus  hyph:E  into  the  rhi/oids,  and  they  believe  that 
the  fungus  whieh  occurs  within  the  thallus  is,  mainly  at  least,  due  to  this  method  of 
infection.  ^>om  a  comparison  with  the  early  infection  of  the  young  prothailium 
in  Ophioglossinn,  it  seems  to  me  more  probable  that  the  young  prothailium  in 
Botrychiitm  also  is  infected  at  a  very  early  period  and  that  the  endophyte,  once 
established  within  its  tissues,  grows  with  the  development  of  the  gametophyte,  the 
secondary  infection  through  the  rhizoids  of  the  older  gametophyte  being  of  minor 
importance. 

In  both  species  of  thjirycluiim  the  infected  region  comprises  the  greater  part 
of  the  central  tissue,  leaving  only  a  comparatively  narrow  peripheral  region  free 
from  the  endophyte.  This  uninfected  area  is  thicker  upon  the  upper  surface  and 
comprises  the  whole  of  the  meristematic  region,  together  with  the  developing  sexual 
organs.  As  in  Ophioglossum,  this  uninfected  tissue  contains  small  starch  granules 
in  considerable  numbers,  but  not  much  else  in  the  way  of  granular  contents.  The 
invasion  of  the  fungus  results  in  the  destruction  of  the  starch  and  the  accumulation 
of  large  amounts  of  oil.  This  oil,  according  to  Jeffrey,  is  not  readily  soluble  in 
alcohol,  and  the  cells  containing  it,  both  in  fresh  and  stained  sections,  appear  dark- 
colored. 

THE  GAMETOPHYTE  OF  HELMINTHOSTACHYS. 

The  monotypic  Heltnitithostachys  zeylanica  is  not  uncommon  throughout  the 
lowlands  of  the  Indo-A4alayan  region  and  often  occurs  in  large  numbers.  The  only 
account  yet  published  of  the  gametophyte  is  that  of  Lang  (Lang  1).  The  prothallia 
which  he  describes  were  collected  in  part  by  himself  in  the  Barrawa  Reserve  Forest 
in  Ceylon  in  March  1901.  Other  material  studied  by  Lang  was  collected  at  the  same 
place  by  Mr.  Coomara  Swamy.  I  made  a  visit  to  the  same  locality  in  February 
1906,  and  also  found  a  considerable  number  of  prothallia,  but  all  of  these  had  been 
fertilized  and  had  attached  to  them  the  young  sporophyte,  so  that  no  young  repro- 
ductive organs  were  found.  The  forest  where  they  were  collected  is  subject  to 
inundation  from  a  river  which  runs  through  it,  and  it  was  in  the  parts  that  had  been 
overflowed  that  the  young  plants  were  discovered.  This  makes  it  not  unlikely  that, 
as  in  the  case  of  Ophioglossum  mohucanuin,  germination  is  favored  by  having  the 
spores  immersed  in  water,  and  this  may  be  a  necessary  condition  for  the  first  stages 
of  germination. 

A  quantity  of  ripe  spores  were  collected  and  various  attempts  were  made  to 
germinate  these,  but  without  success,  and,  as  none  of  the  specimens  obtained  by 
Lang  were  very  y^ung,  the  early  history  of  the  prothailium  still  remains  to  he 
investigated. 

As  in  the  other  Ophioglossace;e,  the  prothallia  are  subterranean,  occurring  at  a 
depth  of  from  5  to  6  centimeters  in  the  earth.  In  form  (figs.  10,  1 1)  they  are  some- 
what intermediate  between  Botrychium  and  Ophioglossum,  but  are  on  the  whole 
more  like  the  latter.  They  are  somewhat  irregular  in  outline,  with  a  broad  base, 
recalling  the  basal  tuber  of  O.  moluccanum,  but  this  tuber  is  relatively  larger  and 
more  lobcd.  From  this  basal  tuberous  portion  a  short  upright  branch  extends, 
much  as  in  Ophioglossum  moUnconum,  but  it  is  relatively  thicker  and  shorter.  The 
whole  gametophyte  is  radial  in  structure,  as  in  Ophioglossum,  and  thus  differs 
strikingly  from  the  dorsiventral  gametophyte  of  Botrychium.  The  basal  enlarged 
portion  is  brown  in  color  and  covered  with  rhizoids,  which  are  mostly  absent  from 
the  upper,  more  slender  part  upon  which  the  reproductive  organs  are  borne. 

Lang  found  that  there  is  a  tendency  to  dicecism  in  the  prothallia,  some  pro- 
ducing only  antheridia  (figure   11,  A),  while   in   others  archegonia  predominate, 


20  THE    OPHIOGLOSSALES 

although  in  the  hitter  a  few  anthcridia  are  almost  always  developed  before  the  arche 
thallium    the    basa 


gonia  appear. 
In  the   mal 


1  "vegetative"  portion  is  relatively  small 
and  often  is  irregularly  lobed,  these  lobes 
being  not  of  the  nature  of  true  branches, 
but  merely  the  result  of  unequal  growth. 
I'he  female  gametophyte  (fig.  lo)  has  the 
basal  region  relatively  larger  and  is  even 
more  irregular  in  form  than  the  male, 
while  the  fertile  region  is  shorter  and 
wider.  Some  of  the  more  elongated  types 
of  the  male  gametophyte  are  quite  similar 
to  the  simple  prothallium  of  Opiuoglossiini 
moluccainim.  As  in  the  other  genera,  the 
endophytic  fungus  is  always  present  and 
occupies  much  the  same  position  as  in 
Botrychium. 

Lang  found  that  the  growth  is  due 
to  the  activity  of  a  single  apical  cell  having 
the  form  of  a  four-sided  pyramid,  much 
like  that  found  in  Ophioglossiim  pendulum. 
1  he  lateral  segments  divide  by  periclinal 
walls,  and  from  the  superficial  cells  thus 
formed  originates  the  layer  of  tissue  from 
which  the  sexual  organs  arise.  The  inner 
cells  contribute  to  the  axial  tissue  of  the 
gametophyte.  The  antheridia  in  the  male 
plants  are  evenly  distributed  about  the 
periphery,  so  that  in  cross-section  they  form 
a  nearly  uniform  circle.  The  axial  tissue, 
^  especially  in  the  male  prothallium,  has  the 

cells    much    elongated,    and    Lang    thinks 
nduction  of  plastic  material  from  the  basal  region  of  the 
prothallium  to  the  growing  point. 

The  outer  part  of  the  basal  region  consists  of  two  or  three  layers  of  somewhat 
flattened  cells,  which,  like  the  corresponding  tissue  in  5o/rv( /;;»»/,  are  free  from  the 
endophyte.  From  some  of  these  superficial  cells  there  are  developed  unicellular, 
elongated  rhizoids,  with  markedly  cutinized  walls.  This  cutinization  extends  to 
the  outer  walls  of  the  superficial  cells,  while  the  inner  walls  of  these  cells,  as  well  as 
those  of  the  inner  tissue,  show  the  cellulose  reaction.  The  formation  of  the  lobes 
of  the  basal  region  are  due,  not  to  definite  apical  growth,  but  to  irregular  cell  divi- 
sions in  the  outer  layers,  which  remain  free  from  the  fungus  which  occupies  the 
greater  part  of  the  central  region  of  the  lobes,  as  well  as  the  axis  ot  the  main  shoot 
of  the  prothallium. 

The  central  tissue  is  made  up  of  about  equal  parts  of  infected  and  uninfected 
cells.  The  latter,  as  in  the  other  cases  investigated,  contain  starch  granules  which 
are  absent  from  the  cells  harboring  the  fungus.  Fungus  hyphae  were  seen  in  many 
cases  to  penetrate  the  rhizoids,  but  it  is  highly  probable  that  in  Helmmthostachys 
also  there  is  a  primary  infection  at  an  early  stage  in  the  germination  of  the  spores. 

Lang  notes  that  in  the  older  male  prothallia  the  fungus  is  dead  and  the  further 
growth  of  the  prothallium  is  dependent  upon  the  amount  of  reserve  food  (mainly 


achys  zeylanica, 
riniary  root.  X 
I'veloped  second 


they  are  useful  in  the 


1HI-:   c;,\Mi 


)1'1IVI 


21 


starch)  \vhi(.h  is  lift  in  tlu-  iills.  It  is  not  clear  wliar  mic  the  enddpliyte  pla\s  in 
the  inaniifactiiie  ot"  the  reserve  food  materials  upon  which  the  further  growth  of  the 
prothalliiim  depends.  It  is  highly  prohaiile,  however,  that  some  of  the  necessary 
organic  elements  are  derived  from  the  destruction  of  the  fungus  tissues  which  serve 
as  food  foi  rhi'  tinther  development  o{  the  prothallium.  While  no  data  are  at  hand 
to  jiroxe  this,  tlu-  lack  of  permanent  growing  tissue  in  the  prothallium  and  the  com- 
plete destruction  of  the  fungus  make  it  highly  probable  that  the  life  of  the  gameto- 
phyte  in  H rIiuiiitli<K<tiii  hxs  is  restricted  to  a  single  season,  as  it  is  in  Ophioglossum 
moluccnnutn. 


of  Helmhlho^tmh- 


:.      X8.        C  Surface  view  of  ripe  antlieriJium,  showing  opercular  cells 
U.  An  old  archegoniiuii.    X  about  200. 
(Figs.  A-C.  after  Lanj;.) 


rilK  F.MXJl'inTK. 

Ihe  endophytic  fungus  which  inhabits  the  gametoph\re  in  all  of  the  Ophio- 
glossaceae  is  very  much  alike  in  all  of  the  species,  differing  only  slightly  in  size  in 
different  forms  (fig.  9).  A  special  study  was  made  of  this  endophyte  in  Ophio- 
glossum pendulum,  where  it  is  especially  well  developed.  As  we  have  already  seen, 
the  endophyte  is  absent  from  the  younger  parts  of  the  prothallium,  but  in  the  older 
parts  it  is  exceedingly  conspicuous.  Sometimes  fiagments  ot  a  fungus  are  found 
outside  the  prothallium,  growing  in  the  humus,  antl  these  are  evidently  the  same 
forms  that  infect  the  very  young  prothallium  when  it  arises  from  the  germinating 
spores.  These  external  hyphre  in  some  cases  have  an  occasional  septum,  and  this 
is  also  the  case  in  those  forms  which  infect  the  young  prothallium.  In  all  of  the 
hyphae  seen  within  the  prothallium,  however,  these  septa  seem  quite  absent.  The 
infection  of  the  prothallium  through  the  rhizoids  has  been  noted  in  all  the  species, 
but,  as  we  have  already  stated,  it  is  probable  that  the  endophyte  is  derived  mainly 
from  the  first  infection  of  the  very  young  gametophyte.  An  examination  of  the  young 
cells  before  the  entrance  of  the  fungus  shows  a  conspicuous  nucleus  and  numerous 
starch  grains,  which  stain  ver\-  strongly  with  gentian  violet.  The  invading  mycelium, 
whither  from  the  outsiiK'  of  the  prothallium  or  tVom  the  adjacent  cells,  peiieriates 
the  cell  wall  and  laiiiihes  within  the  cell,  the  growth  being  entirel\-  intracilhilar. 
The  h\ph;e  are  noticeabU'  thicker  than  those  of  the  external  mycorrhi/a. 

The  endophyte  is  perfectb'  fixed  with  I  per  cent  chromic  acid  antl  it  stains 
well  with  the  double  stain  of  gentian  violet  and  safranine.  the  walls  assuming  a 
violet  color  and  the  niinuTous  niulei  staining  deep  red.  In  the  \dungei  h\  ph;e, 
which  are  of  \ar\ing  sizes,  tin   prot()|ilasni  is  lieiisely  granular,  but  in  the  older  ones 


22  THE    OPHIOGLOSSALES 

the  granular  appearance  disappears  to  a  considerable  extent,  though  the  nuclei 
continue  to  stain  strongly.  The  fungus  is  quite  variable  in  form.  Sometimes  the 
filaments  are  nearly  straight,  running  from  cell  to  cell  and  branching  sparingly. 
Sometimes  a  cell  is  completely  filled  with  a  dense  tangle  of  hyphae,  while  in  other 
cases  there  are  sack-like  vesicles  of  very  irregular  form.  Not  infrequently,  quite 
regular,  nearly  globular  bodies  are  seen,  recalling  the  oogonia  of  the  Peronosporeae. 
These  at  first  contain  comparatively  few  nuclei,  scattered  through  the  granular 
cytoplasm,  but  in  the  older  ones  the  nuclei  are  very  numerous  and  decidedly  larger. 
It  looks  sometimes  as  if  this  were  a  preparation  for  the  formation  of  spores,  but  no 
certain  evidence  of  the  formation  of  such  spores  could  be  seen,  although  in  several 
instances  there  was  an  appearance  which  might  point  to  this.  Structures  resembling 
the  "conidia,"  described  by  Jeffrey  for  Botrychium  (Jeffrey  I,  page  12),  were  seen 
and  are  probably  the  same  thing. 

As  the  fungus  invades  the  young  cells,  irregular,  strongly-staining  clumps  are 
formed  by  the  aggregation  and  breaking  down  of  the  starch  grains.  The  nucleus 
of  the  host  cell  appears  to  be  but  slightly  affected  by  the  growth  of  the  fungus,  and 
can  usually  be  found  quite  unchanged,  even  in  those  cells  which  are  almost  com- 
pletely filled  by  the  endophyte.  Finally,  the  thin-walled  vesicular  growths  of  the 
fungus  are  quite  broken  down  and  probably  serve  to  nourish  the  cells  of  the  gameto- 
phyte,  which  is  thus  parasitic  upon  the  cells  of  the  fungus.  The  systematic  position 
of  the  fungus  is  doubtful.  The  varicose,  swollen  hyphae  found  at  certain  stages 
closely  resemble  a  parasitic  fungus,  Completoria  complens,  which  is  sometimes 
extremely  destructive  to  green  fern  prothallia.  The  obgonium-like  organs,  often 
present,  suggest  Pythium,  a  parasitic  fungus  belonging  to  the  Peronosporeae. 
Jeffrey  (Jeffrey  1,  page  13)  thinks  the  endophyte  may  fairly  be  regarded  as  an 
intermediate  form  between  the  two  genera,  Completoria  and  Pythium,  and  says  that 
in  this  case  Completoria  should  be  placed  in  the  Peronosporeae  instead  of  in  the 
Entomophthoreae,  where  it  has  been  placed  by  some  students  of  the  Fungi. 

THE  SEXUAL  ORGANS. 

THE  ANTHERIDIUM 

The  antheridium  in  all  of  the  Ophioglossaceae  is  of  much  the  same  type  and 
closely  resembles  that  of  the  Marattiaceae  and  also  Equisetum  and  Lycopodium. 
The  mother  cell  does  not  project  at  all  above  the  level  of  the  adjacent  tissue,  and  in 
all  cases  the  first  division  separates  a  superficial  or  cover  cell  from  an  inner  one,  the 
latter  by  further  divisions  giving  rise  to  a  mass  of  sperm  cells  which  may  be  very 
numerous.  The  cover  cell  also  divides,  sometimes  only  in  one  plan,  sometimes 
(e.  g.,  in  Botrychium)  having  also  periclinal  divisions.  At  maturity  the  antheridium 
may  project  more  or  less  strongly,  but  this  is  not  always  the  case. 

THE  .ANTHERIDIUM  OF  OPHIOGLOSSUM 

The  antheridium  was  first  described  by  Mettenius  in  Ophioglossum  pedunculo- 
sum,  and  later  Lang  described  it  for  O.  pendulum  and  Bruchniann  for  O.  vulgatum. 
The  present  account  is  based  mainly  upon  my  own  studies  of  0.  moluccanum  and 
0.  pendulum. 

The  mother  cell  of  the  antheridium,  which  may  arise  very  close  to  the  growing 
point  of  the  prothallium,  lies  flush  with  the  neighboring  cells,  but  later  it  may 
become  more  or  less  elevated  above  the  surface,  forming  a  prominence  which,  in 
slender  prothallia,  like  those  of  Ophioglossum  moluccanum,  may  give  an  irregular 
undulate   outline   to  the   branch    which    bears   them   (fig.  4,  A).      In  ().  pendulum 


THE    GAMETOPHYTE 


23 


this  projection  is  less  marked,  although  this  may  be  somewhat  decided  in  the 
ripe  antheridium.  The  first  division  in  the  inner  cell  is  usually  vertical,  but  may  be 
transverse,  at  least  in  O.  pendulum  (fig.  13,  //).  The  second  walls  intersect  the 
first  at  right  angles,  and  there  are  always  four  nearly  equal  inner  cells  resulting 
(fig.  13,  D).  The  third  set  of  walls  is  vertical,  and  the  next,  in  some  cases  at  least, 
is  in  the  same  direction.  This  is  not  true,  however,  of  the  deeper  and  narrower  type 
of  antheridium.  Further  divisions  occur  until  the  number  of  spermatocytes  is  very 
large.  The  fully  developed  mass  of  spermatocytes  is  plainly  visible  to  the  naked 
eye,  and  in  O.  pendulum  may  reach  a  diameter  of  more  than  325  /x.  250  cells  and 
upward  may  be  counted  in  a  single  section  of  a  large  antheridium,  and  this  would 
mean  that  there  are  several  thousand  in  the  whole  antheridium — perhaps  more  than 
in  any  other  Pteridophyte.  In  O.  moluccanum  (fig.  12),  the  number  of  spermatocytes 
is  much  smaller,  while  in  this  regard  the  antheridium  of  O.  vulgtitum  appears  to  be 
intermediate  between  that  of  0.  moluccanum  and  O.  pendulum. 


I'lG.   ll.—  Oph, 

A.  Ripe  antheridium.     Xi8o. 

B,  C.  Young  antheridia.     X320. 

D.  Surface  view  of  antheridium,  showing  opercular  cell. 


The  nuclei  of  the  young  cells  show  a  conspicuous  nucleolus,  which  becomes  less 
marked  in  the  later  stages  of  the  antheridium.  According  to  Mettenius,  the  outer 
wall  of  the  antheridium  in  0.  pedunculosiim  is  composed  of  two  layers  of  cells;  but 
both  Lang  and  Bruchmann  found  that  the  central  part  of  this  outer  wall  of  the 


I  in  Ophioglossum  pcnduiun 

A.  Median  section  of  gametophyte,  apei,  showing  apical  cell,  x,  and  two  youn 

B.  Transverse  section  of  apex;  x,  apical  cell. 

C.  D.  Median  sections  of  young  antheridia. 

E.  Median  section  of  a  nearly  ripe  antheridium. 

F.  Surface  view  of  ripe  antheridium;  o,  opercular  cell. 


antheridia,  3.    X175. 


24 


THE    OPHIOGLOSSALES 


antheridium  is  but  one  cell  in  thickness,  and  I  have  verified  this  for  both  of  the 
species  under  consideration. 

The  first  wall  to  be  formed  in  the  cover  cell  is  a  nearly  median  one  and  vertical 
(fig.  12,  B),  and  this  is  followed  by  a  second  wall  which  intersects  it,  as  well  as  one 
of  the  lateral  walls  of  the  primary  cover  cell,  so  as  to  include  a  nearly  triangular  cell. 
In  this  triangular  cell  there  are  later  formed,  as  both  Bruchmann  and  Lang  showed, 
a  varying  number  of  segments  arranged  spirally  in  the  fashion  of  the  segments  of  a 
three-sided  apical  cell  (fig.  13,  F).  The  same  thing  occurs  in  Lycopodium  (Treub  1). 
I  have  also  found  a  similar  condition  in  the  antheridium  both  of  the  Marnttiaceae 
and  q{ Equisetuw.  The  last-formed  triangular  cell  is  the  opercular  cell  (fig.  13,^,0). 
From  the  prothallial  tissue  which  adjoins  the  sperm  cells  are  cut  off  flattened  cells 
which  surround  the  sperm  cells  with  a  more  or  less  definite  layer  of  "mantle"  cells. 
The  limits  of  the  original  cover  cell  are  usualh'  plainK'  visible  in  both  longitudinal 
and  surface  sections. 

THK  ANTHERUJU'M  OF  BOTRVCHIUM. 

The  antheridia  in  Botrychiuw  occur  only  upon  the  dorsal  surface  of  the  gam- 
etophyte,  which  is  always  monoecious.  The  first  antheridia  in  B.  virginianiim  (see 
Jeffrey  1,  page  8),  form  a  small  cluster  which  is  not  noticeably  raised  above  the 
general  level  of  the  prothallium,  and  from  this  primary  cluster  extends  a  single 
median  line  of  antheridia  toward  the  apex  of  the  gametophyte.  Later  this  median 
region  becomes  raised  and  forms  a  conspicuous  ridge  along  whose  crest  the  anthe- 
lidia  are  borne.  In  B.  Innarin,  according  to  Bruchmann,  the  arrangement  is 
much  the  same. 


A-D.  Longitudinal  sections  of  young  antheridia. 

E-H.  Transverse  sections.    F,  G  show  only  the 

cell,  0.    I,  section  of  two  ripe  antheridi; 


H,  surface  view  showing  opercul.i 


The  development  of  the  antheridium  is  very  much  like  that  of  Ophioglossum. 
The  first  division,  as  in  the  latter,  is  a  periclinal  one,  separating  the  primary  cover 
cell  from  the  mother  cell  of  the  spermatocytes.  The  divisions  in  the  cover  cell, 
however,  (lifter    somewhat    from   those   in  OphiooJossinn,  in  that  periclinal  walls 


Library 
N.  C,  State  College 


THE    GAMI-TOPHV 


25 


are  formed  in  some  of"  tluse,  so  thar  tlic  eover  Ikcoiiks  to  some  extent  double. 
Jeffrey  states  that  the  cover  is  two  layers  throui^liout,  hut  Hruchmann  found  that 
some  of  the  cells — two  and  sometimes  three — remain  undivided  and  that  one  of 
these  undivided  cells  functions  as  the  opercular  cell.  I  have  examined  this  point 
carefully  in  Botrycliinm  virgiiiianum  and  find  that  there  is  an  opercular  cell  in  this 
species  also.  The  division  walls  in  the  primary  cover  cell  usually  intersect  at  right 
angles,  so  that  the  opercular  cell  is  four-sided,  instead  of  triangular,  as  in  Op/iio- 
glossum  (fig.  14,  H);  but  exceptionally  it  may  have  the  triangular  form.  In  the 
dehiscence  of  the  antheridium  only  a  single  opercular  cell  is  destroyed,  not  two 
superimposed  cells,  as  Jeffrey  supposed  to  be  the  case. 

The  divisions  in  the  central  cell  are  very  much  the  same  as  in  Opiiioglossiim. 
Whether  the  first  division  is  regularly  transverse  or  vertical  could  not  be  determined, 
as  no  examples  of  the  first  division  were  found.  The  earliest  stages  seen  after  the 
first  separation  of  the  cover  cell  had  four  inner  cells  arranged  quadrant-wise,  but 
it  was  not  clear  which  was  the  primary  wall.  The  quadrant  division  is,  usuall)'  at 
least,  followed  by  an  octant  division,  and  these  earh'  divisions  may  sometimes  be 
recognized  for  a  long  while,  as  there  is  not  nuich  displacement  of  the  cells  due  to  the 
subsequent  divisions.  In  the  later  stages  the  primary  divisions  can  no  longer  be 
made  out  clearly.  The  number  of  sperm  cells  finally  formed  may  be  very  large — 
more  than  a  thousand  in  the  largest  antheridia  thus  nearh'  or  quite  equaling  the 
number  found  in  Opliioglossiun  pcndiiliiin,  although  the  speini  cells  are  very  much 
less  in  size  than  in  the  latter  and  the  antheridium  correspondingly  smaller.  Some- 
times the  antheridium  is  divided  into  irregular  chambers,  apparently  due  to  the 
persistence  of  some  of  the  early  division  walls  (fig.  15,  B). 


Fig.  15. — Bolrychium  virgwu 

A.  Longituilin.-il  section  of  a  nearly  ripe,  but  rather  small,  antheridium.     X  about  200. 

B.  Section  of  a  ripe  antheridium  which  has  discharged  the  spermatozoids;  some  cell-walls  have  remained, 

forming  irregular  chambers,  and  retaining  some  of  the  spermatozoids. 

C.  A  surface  view  of  a  ripe  antheridium,  showing  square  opercular  cell. 

The  antheridium  of  B.  lunaria,  according  to  Bruchmann,  is  smaller  than  that 
of  5.  virginianiini,  but  the  size  of  the  spermatocytes  and  spermatozoids  seems  to  be 
about  the  same  (fig.  8,  D). 

THE  ANTHERU)UM  Ol'  HLI.MIXTHOSTACHVS. 

The  antheridium  of  H clmitilhostdrhys  has  been  studied  by  Lang,  and  it  is 
evident  from  his  account  that  it  resembles  that  of  BcArychimn  much  more  than  it 
docs  that  of  Opiuoglossnni.  As  in  the  former,  the  primary  cover  cell  undergoes 
periclinal  divisions  as  well  as  anticlinal  oiu  s,  bur  there  are  from  two  to  four  cells 
which  do  not  divide  by  periclinal  walls,  and  oiu  of  these  cells  becomes  the  opercular 
cell  (fig.  I  I,  (J).  Thise  four  umlividt-d  cells  stain  more  strongh'  than  the  other  cells 
of  the  cover,  bur  onU  oiu'  of  rluni  is  broken  down  at  ihr  time  of  deliisceiuT.     These 


26  THE    OPHIOGLOSSALES 

cells,  as  in  the  case  of  Botryihiiini  Itiiuuia,  are  nearly  square  in  outline,  most  of  the 
walls  in  the  cover  cells  being  at  right  angles  to  each  other,  as  in  BrArychium. 

The  divisions  in  the  central  cell  are  very  similar  to  those  in  Ophioglossum  and 
Botrychium,  and  the  original  quadrant  divisions  are  perceptible  for  some  time. 
The  number  of  spermatocytes,  as  in  Ophioglossum  and  Botrychium,  may  be  very  large. 
The  spermatozoids  were  not  seen  by  Lang,  but  from  a  comparison  of  the  nuclei  of 
the  spermatocytes  they  are  apparently  of  about  the  same  size  as  those  of  Botrychium. 

SPERMATOGENESIS. 

Ophioglossum  is  especially  suited  to  a  study  of  spermatogenesis,  owing  to  the 
very  large  size  of  the  spermatozoids.  Those  of  0.  pendulum  are  probably  the 
largest  known  among  the  Pteridophytes.  In  material  fixed  with  i  per  cent  chromic 
acid,  or  weak  Flemming's  solution,  and  stained  with  gentian  violet  and  aniline 
safranine,  the  coloring  is  beautifully  clear  and  the  blepharoplast  stains  with  extra- 
ordinary sharpness.  The  spermatozoids  of  O.  pendulum  are  larger  than  those  of 
O.  moluccanum  or  O.  vulgatum,  but  the  development  is  very  much  the  same. 

If  the  sperm  cells  are  examined  previous  to  the  final  division  to  form  the 
spermatocytes  (plate  i,  fig.  i6),  the  nucleus  will  be  seen  to  have  a  small  but  distinct 
nucleolus  and  a  dense  reticulum.  The  whole  nucleus  stains  strongly  with  safranine. 
The  cytoplasm  is  fairly  dense,  with  granules  of  various  kinds  in  it.  In  material 
fixed  with  Flemming's  solution  there  are  often  small  black  specks,  probably  fatty 
bodies,  which  sometimes  interfere  somewhat  with  the  study  of  the  cytoplasm.  In 
well-stained  sections  the  blepharoplasts  may  be  seen  as  tw^o  small,  rounded  bodies 
of  a  violet  color  (plate  i,  fig.  i6,  hi)  lying  near  the  nucleus.  Several  cases  of  the  final 
nuclear  divisions  were  met  with,  but  all  of  these  were  in  material  fixed  with  chromic 
acid,  and  the  blepharoplasts  were  not  very  well  difl^erentiated  (plate  2,  fig.  22).  The 
nuclear  spindle  is  very  distinct,  and  the  very  numerous  chromosomes  are  so  crowded 
that  it  was  quite  impossible  to  determine  their  number  exactly,  but  it  is  very  large. 
In  the  young  spermatocytes  (plate  2,  fig.  26)  the  nucleus  shows  a  more  or  less  con- 
spicuous reticulum,  but  the  nucleolus  has  disappeared,  as  it  usually  does  at  this 
stage  in  all  the  forms  that  have  been  studied.  The  further  development  of  the 
spermatozoid  coTresponds  very  closely  with  that  of  Equisetum  (see  Campbell  4  and 
BelajefF  1,  2).  One  of  the  blepharoplasts  in  the  primary  spermatocyte  goes  with 
each  daughter  cell  (the  definitive  spermatocyte)  and  can  be  seen  as  a  distinct  rounded 
body  lying  near  the  nucleus  (plate  2,  fig.  24).  In  some  cases  what  appeared  to  be 
the  blepharoplast  was  lying  in  a  depression  at  the  periphery  of  the  nucleus,  and 
looked  very  much  like  a  nucleolus. 

Before  the  nucleus  undergoes  any  marked  change,  the  blepharoplast  begins 
to  elongate  (plate  2,  figs.  26,  27)  and  assumes  the  form  of  a  pointed,  slender,  strongly 
staining  body  lying  near  the  nucleus.  This  body  is  really  somewhat  ribbon-shaped, 
and  more  pointed  at  one  end  than  the  other,  and  it  is  also  somewhat  curved,  even 
in  its  earlier  stages.  A  transverse  section  appears  crescent-shaped.  The  nucleus 
now  elongates  slightly  and  the  reticulate  structure  becomes  very  conspicuous  (plate 
2,  fig.  25).  There  are  large,  strongly  stained  granules,  which  are  probably  composed 
of  several  more  or  less  coherent  chromosomes,  as  the  number  of  these  granules  is 
very  much  less  than  the  number  of  chromosomes  in  the  nuclear  plate  of  the  dividing 
nucleus.  The  blepharoplast  continues  to  elongate,  and  in  favorable  cases  the  young 
cilia  can  be  seen  growing  from  it,  but  none  of  my  preparations  showed  the  cilia 
nearly  so  plainly  as  Belajeff's  figures  show  them  in  Equisetum  and  Gymnogramme. 
There  is  no  doubt,  however,  that  the  cilia  arise  in  much  the  same  way  as  BelajefF 
describes.    The  nucleus  now  becomes  indented  on  one  side  and  assumes  a  crescent 


THE    GAMETOPHYTE  27 

shape,  elongating  and  also  becoming  nioif  or  kss  flattencti.  One  end  becomes 
narrower  and  sharply  pointed,  the  other  remaining  thicker  and  rounded.  The 
reticulum  at  this  time  stains  with  great  intensity  and  shows  a  tendency  to  coalesce, 
which  in  the  final  stage  results  in  an  almost  homogeneous,  deeply-staining  mass, 
composed  apparently  of  the  completely  fused  chromosomes.  In  successful  prepara- 
tions the  nucleus  at  this  stage  stains  a  clear  carmine  red,  in  strong  contrast  to  the 
bright  violet  of  the  blepharoplast.  With  the  complete  coalescence  of  the  chromo- 
somes the  volume  of  the  nucleus  is  noticeably  decreased  (plate  i,  fig.  19).  The 
blepharoplast  forms  a  spirally  coiled  narrow  band,  from  which  the  cilia  can  be  seen 
to  grow,  following  its  curve,  but  the  blepharoplast  is  not  in  close  contact  with  the 
nucleus. 

i'he  spermatocytes  and  the  nuclei  are  rather  smaller  in  (Jphioglossiirn  moluc- 
camtm  than  in  O.  pendulum.  In  the  older  stages  of  the  spermatozoid,  the  nucleus 
in  the  former  species  is  decidedly  more  elongated  and  more  sharply  pointed  at  both 
ends  (plate  i,  fig.  18).  In  this  respect  it  more  nearly  resembles  the  spermatozoids 
of  Botrychiurn  and  those  of  the  true  ferns;  while  in  the  larger,  comparatively  short 
nucleus,  as  well  as  in  some  other  respects,  the  spermatozoid  of  O.  pendulum  is  strik- 
ingly like  that  of  Equisetum.  Ihe  number  of  cilia  is  large,  but  the  exact  number 
could  not  be  determined. 

Surrounding  the  spermatozoid  and  included  in  its  coils  is  a  considerable  amount 
of  cytoplasm.  I  was  not  successful  in  obtaining  any  living  spermatozoids,  although 
many  attempts  were  made  to  do  this,  but  in  a  number  of  sections  of  the  opened 
antheridium  some  were  found  in  which  the  spermatozoids  had  been  retained.  While 
these  were  usually  more  or  less  distorted,  some  were  very  well  fixed  and  gave  a  good 
idea  of  the  structure  of  the  free  spermatozoid  (plate  2,  fig.  28).  The  cilia  were 
very  much  distorted  in  some  cases,  but  in  some  they  were  clearly  seen.  Ihere  is 
one  thick  posterior  coil  mainly  composed  of  the  nucleus,  which  is  very  much  larger 
than  that  of  the  sperm  cell  before  it  is  discharged  from  the  antheridium.  The 
nucleus  has  the  form  of  a  slightly  coiled  thick  band,  tapering  somewhat  at  both  ends, 
but  more  markedly  so  in  front.  Beyond  this  extends  a  second  coil,  composed, 
apparently,  mainly  of  cytoplasm.  1  his  second  coil  extends  into  a  third  much  smaller 
one,  which  seems  to  be  a  flattened  band  along  whose  upper  edge  the  blepharoplast  is 
closely  applied  (plate  2,  fig.  28).  The  resemblance  of  the  spermatozoid  to  that  of 
Equisetum  is  very  strong,  but  the  nucleus  is  even  more  shortened  than  in  the  latter. 

The  spermatozoid  ofOphioglossum  pendulum  is  larger  than  that  of  any  Pterido- 
phyte  that  has  yet  been  described.  The  cytoplasmic  envelope  and  vesicle  are  not 
very  clearly  separated  and  probably  are  similar  to  those  of  the  free  spermatozoids 
of  O.  vulgatum  or  o{  Equisetum.  Sometimes  this  protoplasmic  envelope  completely 
surrounds  the  lower  part  of  the  spermatozoid  and  reminds  one  somewhat  of  the 
peculiar  spermatozoids  of  the  Cycads.  Owing  to  their  large  size,  the  spermatozoids 
were  often  sectioned,  and  in  some  of  the  sections  the  blepharoplast  was  free  from 
the  body  of  the  spermatozoid  and  the  attachment  of  the  cilia  was  very  easily  seen 
(plate  2,  fig.  29,  a). 

Mettenius  figures  the  free  spermatozoids  of  O.  pedunculosum,  but  his  figures 
are  certainly  not  accurate.  Bruchmann,  who  has  figured  those  of  ().  vulgatum 
(fig.  5,  D),  shows  that  they  closely  resemble  the  spermatozoids  of  the  true  ferns,  but 
are  more  massive,  and  the  vesicle  which  envelops  the  posterior  coils  adheres  more 
closely  to  the  spermatozoid  than  is  usual  in  the  terns.  In  these  respects  it  resembles 
the  spermatozoid  of  ().  pendulum. 

Jeffrey  examined  the  development  of  the  spermatozoids  in  Botrychium  vn- 
ginidnum,  which  closely  resemble  those  of  Ophioglossum.    Owing  to  the  method  of 


28  THE    OPHIOGLOSSALES 

Staining  which  he  employed,  the  blepharoplast  was  not  clearly  evident.  I  have 
examined  the  developing  speimato/oids  in  this  species,  using  the  material  which 
Professor  Jeffrey  was  so  kind  as  to  send  me,  but  employing  the  double  stain  of 
safranine  and  gentian  violet,  which  was  used  in  the  study  of  Ophioglossum.  While 
the  differentiation  was  inferior  to  that  of  Ophioglossum,  where  the  material  was 
fixed  with  Flemming's  solution,  nevertheless  the  presence  of  the  blepharoplast  was 
unmistakable. 

The  spermatocytes  are  only  about  half  as  large  as  those  of  Ophioglossum 
pendulum,  and  the  spermatozoids  correspondingly  smaller;  hence  less  favorable 
for  the  study  of  details.  It  is  evident,  however,  that  the  changes  in  the  nucleus  and 
blepharoplast  are  essentially  the  same  as  in  Ophioglossum  (plate  2,  figs.  34  to  37). 
The  nucleus,  however,  becomes  much  more  elongated  and  the  spermatozoids  are 
more  slender,  in  both  of  which  respects  it  shows  a  resemblance  to  the  spermatozoids 
of  the  typical  ferns. 

The  study  of  the  free  spermatozoids  was  confined  to  those  which  happened  to 
have  become  fixed  within  the  open  antheridium  and  within  the  venter  of  recently 
opened  archegonia.  These  were  in  some  cases  very  satisfactorily  fixed  and  stained, 
and  showed  very  well  indeed  the  general  form  of  the  spermatozoid.  The  cilia, 
however,  were  not  as  a  rule  very  well  fixed,  and  while  they  are  evidently  numerous 
their  number  could  not  be  made  out. 

Bruchmann's  figures  (fig.  8,  D)  of  the  free  spermatozoid  o'i  Bo1r\ihiinu  lunaria 
agree  closely  in  form  and  size  with  those  of  B.  virgiuianum.  In  both  species  the 
vesicle  attached  to  the  spermatozoid  is  more  distinct  than  in  Ophioglossum,  and 
in  this  respect  also  the  spermatozoid  shows  a  likeness  to  the  true  ferns. 

TH1-;  ARCHEGONIl'M. 

The  archegonium  in  the  Ophioglossaceae  is  very  much  like  that  of  the  typical 
ferns  in  its  general  development.  The  mother  cell  of  the  archegonium,  like  that  of 
the  antheridium,  is  first  divided  by  a  periclinal  wall  into  an  outer  cover  cell,  which 
later  gives  rise  to  the  four  rows  of  neck  cells,  and  an  inner  cell  which,  as  in  the  typical 
ferns,  divides  again  by  a  transverse  wall  into  a  lower  or  basal  cell  and  a  central  cell, 
the  latter  subsequently  giving  rise  to  the  egg  cell  and  the  canal  cells.  A  marked 
feature  m  the  archegonium  of  the  Ophioglossaceae  is  the  inconspicuous  character 
of  the  ventral  canal  cell,  which  very  often  it  is  impossible  to  show,  and  it  is  possible 
that  in  some  cases  the  ventral  canal  cell  may  not  be  formed  at  all,  although  I  think 
this  is  doubtful.  In  general  the  archegonium  is  much  alike  in  the  three  genera,  but 
the  neck  is  much  shorter  irr  Ophioglossum  than  in  Botr\chium  or  Hrlmiiitiiostaihys. 

THE  ARCHEGONUM  OF  OPHIOGLOSSUM. 

My  own  studies  of  the  development  of  the  archegonium  of  Ophioglossum  were 
based  mainly  upon  a  study  of  Ophioglossum  pendulum.  Only  a  very  small  number  of 
the  young  archegonia  was  secured  in  O.  moluccanum,  and  so  it  was  impossible  to 
make  a  complete  study  in  this  species.  Lang  accurately  figures  several  stages  of 
the  archegonium  in  Ophioglossum  pendulum,  and  Bruchmann  has  described  quite 
completely  its  development  in  O.  vulgatum.  Bruchmann  failed  to  see  the  two 
nuclei  of  the  neck  canal  cell  which  Lang  correctly  figures  for  0.  pendulum.  Fhese 
two  nuclei  are  invariably  present  in  both  0.  pendulum  and  0.  moluccanum,  and  it 
is  to  be  expected  that  they  will  also  be  found  in  O.  vulgatum,  as  they  are  constantly 
present  also  in  Botrychium  virgiuianum  and  in  all  of  the  ferns  that  have  been 
accurately  examined.  Neither  Lang  nor  Bruchmann  saw  the  ventral  canal  cell, 
which  is  exceedingly  difficult  to  demonstrate. 


TH1-:    GAMKTOI'IIV 


In  ()i^lii<,olnssinu  tin-  \cum<;  ;iirlHi;nni;i  m;i\  lie  tniiiul  lu.ii  thr  ,i|nx  ot  tin- 
pi<.tlialli;il  hi;nuh,  Inir  tluy  m;iv  als.i  ."iiisc-  ;it  .1  coiisidtiiilik-  ilistaiur  liack  nf"  it. 
In  mniial,  liki-  the  antheiidia,  tlu\   ailsc  in  atrc)|>ital  succession. 

Ilu-  niiitlifi  cill,  like  that  of  tin-  antlu  mliuni,  is  sometimes  lirnail,  sonutinus 
nairow  and  deep,  and  the  cover  cell  is  conespondini^ly  shallow  or  dee|i.  1  In-  hist 
division  of  the  inner  cell  takes  place  shortly  after  the  cover  cell  is  cut  off.  The  next 
division  is  in  the  cover  cell,  which  Hrst  divides  hy  a  vertical  wall,  a  second  \ertical 
wall  being  formed  almost  immediately,  intersecting  the  first  and  dividing  the  cover 
cell  into  four  practicalh  e(pial  cells,  arranged  quadrant-wise  (fig.  16,  A).  The 
middle  cell  next  divides  by  a  transverse  wall  into  the  primary  neck  canal  cell  and 
the  central  cell  (fig.  16,  /•").  The  canal  cell  pushes  up  between  the  four  primary 
neck  cells,  which  presently  divide  by  nearly  horizontal  walls,  so  that  there  are  two 
tins  of  neck  cells.  One  01  both  of  these  di\  ide  again  later,  so  that  each  row  of  neck 
cells  consists  of  thiee  or  four.  Rareh'  the  re  ma\-  be  Hve  cells  in  one  01  more  of  the 
rows. 


— Development  of  the  archegonium  in  Ophiogloisun, 

\.  Transvcriic  section  of  gametophyte  apex,  showing  two  young  archegonia,? ,  and  apical  cell,  x. 

B-G.  Successive  stages  in  the  development  of  the  archegonium;  seen  in  longitudinal  section;  «,  neck  canal  cell;  b,  b.isal  cell. 

H.  Recently  fertilized  arcliegonium;   5/>,  a  spcrmatozoid  within  the  egg  nucleus. 

The  neck  canal  cell  is  very  conspicuous,  its  base  being  broad,  and  the  upper 
part  narrower  and  extending  to  the  uppermost  neck  cells.  The  large  and  conspicu- 
ous nucleus  soon  divides  into  two,  but  as  a  rule  there  is  no  division  wall,  although 
occasionally  two  distinct  neck  canal  cells  may  be  present.  Sometimes  both  of  the 
nuclei  remain  in  the  broad  basal  part  of  the  cell,  and  sometimes  one  is  at  the  base 
and  one  nearer  the  apex.  This  arrangement  seems  to  depend  upon  the  direction 
in  which  the  nuclear  division  takes  place. 

1  he  basal  cell  divides  by  a  vertical  wall  at  about  the  same  time  that  the  primary 
canal  cell  is  cut  off  from  the  central  cell.  Ihe  basal  cell  subsequentU  undergoes 
further  divisions,  but  its  limits  are  readily  distinguishable  up  to  the  time  that  the 
archegonium  is  mature  (fig.  16,  G). 

In  its  earlier  stages,  the  archegonium  of  Ophioglossitrn  pendiduni  bears  a 
striking  resemblance  to  that  of  the  Marattiacea?,  which  the  mature  archegonium 
more  nearly  resembles  than  it  does  that  oi Botr\chiiim.  According  to  Bruchmann's 
account,  0.  vulgatiini  has  a  neck  somewhat  longer,  and  this  is  also  true  of  O.  mohn- 
ciiniini.  Even  when  mature,  the  neck  projects  but  little  above  the  surface  of  the 
prothallium.  although  there  is  some  elongation  of  the  cells  at  the  time  of  dehiscence 
(fig.  1^'.  (!)■ 

The  venrial  canal  cell  is  ver\-  iliffcult  to  demonstrate,  and  one  is  sometimes 
inclined  to  ilouht  whether  it  is  formed  at  all  in  some  cases;   neither  Lanij  nor   Bruch- 


30 


THE    OPHIOGLOSSALES 


nianii  was  able  to  detect  it  in  ().  pcndiihini  and  O.  vulgatiiiii.  It  is  probable  that 
its  apparent  absence  in  most  ot  the  archegonia  is  due  to  the  fact  that  it  is  formed  very 
late  and  is  extremely  inconspicuous.  The  same  apparent  absence  of  a  ventral  canal 
cell  in  the  Cycads  and  some  Conifers  has  been  shown,  on  more  critical  study  of  the 
material,  to  be  due  to  the  small  size  of  the  ventral  nucleus  and  to  its  very  evanescent 
character.  In  nearly  all  of  the  archegonia  examined,  just  before  they  opened  there 
was  present  a  vesicular  body  above  the  egg,  which  was  probably  the  ventral  canal 
cell  much  distended  with  fluid  preparatory  to  the  opening  of  the  archegonium.  A 
small  nucleus,  or  what  looked  like  one,  could  sometimes  be  seen,  but  it  must  be  said 
that  its  nuclear  nature  was  not  above  suspicion  (plate  2,  fig.  33). 

Just  before  the  archegonium  is  ready  to  open,  the  egg  cell,  which  up  to  this 
time  is  compressed  above  by  the  basal  wall  of  the  neck  canal  cell,  becomes  distended 
and  pushes  up  the  base  of  the  canal  cell,  which  thus  becomes  concave  below.  It  is 
probably  about  this  time  that  the  ventral  canal  cell  is  cut  off.  Unfortunately,  no 
cases  were  found  showing  mitosis  in  the  central  cell,  but  there  seems  no  good  reason 
to  doubt  that  a  ventral  canal  cell  is,  usually  at  least,  cut  off. 


Fig.  17. — Development  of  tlie  archegonium  in  j 

A-D.  Longitudinal  sections.     X320. 

K.  Ripe  archegonium,  showing  ventral  canal  cell  i'.    X 

F.  Recently  fertilized  archegonium,  showing  spcrmatt 


65.     (After  Jeffrey.) 
;oids  within  venter.     X32 


The  neck  canal  cell  does  not  show  the  complete  disorganization  which  is  com- 
mon, but  retains  its  form  up  to  the  time  that  the  archegonium  opens.  With  the 
opening  of  the  neck  there  is  some  elongation  of  the  outer  neck  cells,  but  there  is 
decidedly  less  projection  above  the  surface  of  the  prothallium  in  O.  prmhilutn  than 
is  the  case  in  O.  viilgatnm.  The  nucleus  of  the  egg  cell  is  large,  but  it  does  not  always 
stain  readily,  except  the  nucleoli,  and  it  may  be  that  the  same  resistance  to  stains 
is  the  reason  why  its  sister  nucleus  in  the  ventral  canal  cell  is  so  difficult  to  sec. 


THF,  ARCHEGONIUM  OF  BOTRYCHUmf. 


The  archegonia  in  Botrychltim  are  found  usually  upon  the  flanks  of  the  median 
ridge,  upon  whose  summit  are  borne  the  antheridia.  In  their  early  stages  they 
closely  resemble  those  of  Ophioglossum  (fig.  17).  As  in  the  latter,  there  is  some 
variation  in  the  form  of  the  mother  cell,  which  may  be  quite  deep  and  narrow,  or 
relatively  broad  and  shallow.     The  subsequent  divisions  in  the  central  cell  and  in 


THK    GAMKTOPHVTI-;  31 

the  covL-i  cell  agree  very  closely  with  those  in  Ophioglossinn;  hut  the  neck  cells  arc 
more  numerous  and  at  maturity  the  neck  projects  much  more  strongly  than  is  the 
case  in  Ophioglossum.  There  may  be  as  many  as  seven  or  eight  cells  in  each  row 
of  the  neck,  which,  except  that  it  is  quite  straight,  resembles  that  of  the  typical 
ferns.  It  is  especially  like  that  of  OsmunJd,  in  which  the  neck  is  also  straight.  The 
neck  canal  cell  (fig.  17,  D)  becomes  much  elongated,  and  the  nucleus  divides,  as  in 
Ophioglossum,  but  in  most  cases  at  least  there  is  no  division  of  the  canal  cell  itself. 
As  in  Ophioglossum,  the  ventral  canal  cell  is  very  inconspicuous,  and  often 
impossible  to  detect.  Jeffrey  (fig.  17,  E)  figures  a  very  evident  ventral  canal  cell, 
but  the  nucleus  is  much  smaller  than  that  of  the  egg  or  neck  canal  cell.  I  have  also 
found  what  seemed  to  be  a  ventral  canal  cell  in  the  archegonium  shortly  before  it 
opened,  but,  as  in  the  case  of  Ophioglossum,  this  was  not  absolutely  certain.  As 
in  the  corresponding  stage  in  Ophioglossum,  above  the  egg  cell,  with  its  large  and 
conspicuous  nucleus,  there  is  a  clear  space  containing  a  small  round  body,  which 
showed  no  evident  nucleolus,  but  otherwise  stained  very  much  like  the  nucleus  of 
the  egg,  and  was  probably  the  nucleus  of  the  ventral  canal  cell  (fig.  ij,D,v.) 
While  no  certain  cases  of  mitosis  of  the  egg  nucleus  for  the  cutting  off  of  the  ventral 
canal  cell  were  encountered,  in  one  case  the  egg  nucleus  looked  as  if  it  were  in  the 
early  prophase  of  division.  Bruchmann's  figures  of  the  archegonium  of  Botrychium 
lunaria  closely  resemble  that  of  B.virginianum,  but  he  was  unable  to  find  a  ventral 
canal  cell,  nor  did  he  apparently  see  the  division  of  the  nucleus  of  the  neck  canal  cell. 
The  archegonium  ofHchnint}iostachys{fig.  11, D)  closely  resembles  that  of  Botrychiutn. 

FERTILIZATION. 
In  only  a  few  cases  were  spermatozoids  seen  within  the  neck  and  venter  of  the 
open  archegonium  in  Ophioglossum,  but  twice  a  spermatozoid  was  seen  within  the 
nucleus  of  the  egg;  as  there  were  no  other  stages  obtained,  however,  the  details  of 
nuclear  fusion  could  not  be  followed  (fig.  16,  H).  The  spermatozoid  penetrates 
the  nucleus  of  the  egg,  where  for  a  time  it  can  be  seen  distinctly.  It  is  probable 
that  its  fusion  with  the  egg  nucleus  is  much  like  that  described  by  Shaw  for  Ouoclca 
(Shaw  I,  2).  In  the  mature  egg  cell  the  nuclear  reticulum  is  often  decidedly  con- 
tracted, but  whether  this  is  normal  or  the  result  of  reagents  can  not  be  said. 

FICKTILIZATtON  IN  BOTRYCHIUM  VIKCINIANl'M. 

Jeffrey  observed  a  single  spermatozoid  within  the  venter  of  the  archegonium 
and  noted  that  at  the  time  of  fertilization  the  egg  developed  what  he  called  a 
"  receptive  prominence."  I  have  observed  the  same  phenomenon  in  several  cases 
(plate  2,  fig.  46),  and  in  a  good  many  instances  have  also  found  one  or  more  sper- 
matozoids within  the  venter.  In  one  case,  what  looked  very  much  like  a  sperma- 
tozoid was  seen  within  the  egg  nucleus  itself,  and  the  process  of  fusion  is  probably 
very  much  the  same  as  that  so  fully  described  by  Shaw  for  Ouoclca.  In  the  specimen 
shown  in  fig.  17,  /•,  oneof  the  spermatozoids  looks  as  if  it  has  partially  penetrated 
the  egg,  but  it  is  mipossible  to  be  certain  that  it  was  not  simpl\'  lying  against  it.  In 
this  case,  just  above  the  nulceus  of  the  egg  there  was  a  slight  bicak  in  the  gianular 
cytoplasm  that  looked  as  if  it  might  be  a  receptive  spot,  bur  the  speimatozoitl  was 
not  entering  the  egg  at  this  point. 

In  another  instance  a  curious  thing  was  noted,  but  whether  it  was  normal 
or  not  it  is  impossible  to  sav  (plate  2,  fig.  46).  A  spermatozoid  had  just  entered 
the  neck  of  the  open  archegonium  and  the  egg  had  developed  a  ver\-  conspicuous 
receptive  prominence.  The  nuclear  contents  were  very  strongly  Contracted  and 
deeply  stained  and  a  portion  apparently  projected  beyond  the  nuclear  membrane 


32  THD    OPHIOGLOSSALES 

into  the  receptive  prominence.  A  similar  synapsis  was  noted  in  several  cases.  In 
most  instances  where  free  speimatozoids  were  present  in  the  venter  of  the  arche- 
gonium  the  egg  nucleus  presented  a  curious  appearance  (plate  2,  figs.  47,  48).  A 
single  large  nucleolus  was  present,  but  scattered  through  the  nucleus  there  were 
sometimes  a  dozen  or  more  of  intensely  staining  round  bodies,  which  at  first  sight 
looked  like  nucleoli,  but  on  more  careful  examination  were  seen  to  differ  from 
the  large  nucleolus  in  that  they  appeared  less  homogeneous  and  generally  showed  a 
central  vacuole-like  structure.  These  granules  stain  very  much  like  the  body  of 
the  spermatozoid,  and  it  was  thought  that  possibly  they  might  be  derived  from  a 
fragmentation  of  the  body  of  the  spermatozoid  that  had  entered  the  nucleus,  but 
this  could  not  be  satisfactorily  demonstrated  and  the  nature  of  this  phenomenon 
must  remain  for  the  present  uncertain. 

Fertilization  in  HchnintliostaL-hys  has  not  been  obseived. 

SK;N1F1CANCE  of   the  KNUOI'HYTE. 

That  the  presence  of  the  endophyte  is  essential  to  the  existence  of  the  sapro- 
phytic gametophyte  of  the  Ophioglossaceze  is  indicated  by  the  failure  of  the  germi- 
nating spores  to  develop  unless  they  become  associated  with  the  fungus.  Moreover, 
the  universal  occurrence  of  a  similar  endophyte  in  all  humus  saprophytes  among 
the  seed  plants  indicates  that  in  all  of  these  chlorophyll-less  plants  the  presence  of  the 
fungus  is  necessary  for  the  existence  of  the  host.  Although  it  has  not  been  directly 
proved,  it  is  generally  assumed  that  one  role  of  the  endophyte  is  the  elaboration  of 
some  of  the  carbonaceous  constituents  of  the  humus.  The  infrequent  communica- 
tion between  the  external  hyphae  and  the  internal  mycelium  makes  it  unlikely  that 
the  nutritive  products  are  directly  absorbed  by  the  fungus,  and  it  seems  much  more 
probable  that  the  rhizoids  of  the  gametophyte  are  the  direct  agents  of  absorption. 
How  the  humus  constituents  are  changed  by  the  action  of  the  fungus  so  that  they 
are  available  for  the  cells  of  the  host  is  not  clear,  and  it  is  by  no  means  impossible 
that  some  at  least  of  the  necessary  carbon  may  be  derived  from  the  fungus  itself, 
in  the  digestive  process  to  which  it  is  subjected  in  the  cells  of  the  host.  This  seems 
plausible  from  the  fact  that  in  the  green  prothallia  of  certain  ferns,  where  presumably 
the  gametophyte  is  entirely  able  to  supply  its  own  carbon  compounds  through 
photosynthesis,  these  digestive  cells  appear  to  be  wanting;  at  any  rate  they  were  not 
observed  in  a  number  of  forms  that  I  have  studied. 

The  experiments  of  Ternetz  (Charlotte  Ternetz  I),  show  that  certain  fungi, 
including  endophytic  mycorrhizae,  are  able  to  assimilate  free  nitrogen  and  confirm 
the  assumption  of^  earlier  observers  that  the  fungus  is  useful  to  the  host  in  supplying 
it  with  nitrogen  compounds;  but,  while  this  is  probably  a  very  important  part  of 
its  functions,  it  seems  to  me  that  it  is  not  perhaps  the  only  one,  and  that  the  carbon 
also  is  supplied,  directly  or  indirectly,  through  the  agency  of  the  fungus. 

In  an  extended  study  of  the  endophytic  mycorrhiza  of  the  saprophytic  orchid, 
Neoitin,  W.  Magnus  (W.  Magnus  1)  has  shown  that  two  types  of  mycelium  ex- 
hibited by  the  endophyte  are  of  very  different  nature.  The  slender,  cylindrical 
hyphae  constitute  the  active  portion  of  the  fungus,  which  behaves  like  a  parasite 
toward  the  cells  which  it  invades,  destroying  the  starch  and  probably  other  constitu- 
ents of  the  cells,  but  not  attacking  the  nucleus.  The  swollen  vesicular  mycelium, 
however,  is  a  degenerating  structure  and  is  itself  destroyed  by  the  cells  of  the  host, 
which  actually  digest  these  fungus  mycelia  in  much  the  same  way  that  the  cells  of 
the  leaf  of  Dnsera  digest  their  prey.  Magnus  has  very  graphically  shown  that  the 
relation  of  the  two  symbionts  is  mutually  antagonistic,  each  one  acting  as  a  parasite 
on  the  other;    nevertheless  the  presence  of  the  fungus  is  essential  to  the  higher 


THE    GAMETOPHYTE  33 

ort^aiiisni,  so  long  as  tin-  latter  is  destitute  of  chlorophyll.  Tht-  explanation  of  the 
widespread  saprophytism  exhibited  by  so  many  of  the  higher  plants  may  be  sought 
in  this  attempt  to  defend  themselves  against  what  was  probably  at  first  a  strictly 
parasitic  organism.  Having  acquired  the  power  to  attack  and  to  feed  upon  the 
parasite,  the  photosynthetic  functions  were  more  and  more  subordinated,  until  a 
state  of  true  parasitism  (or  saprophytism)  resulted.  The  numerous  semi-saproph}tes 
like  most  of  the  green  Ericales  and  many  of  the  green  ()rchidace;e,  are  good  examples 
of  transition  stages,  while  the  characteristic  leafless  humus  saproph\tes,  such  as 
iVIonotropa  and  Corallorhlza,  represent  the  fully  developed  phase  of  this  peculiar 
form  of  symbiosis.  We  might  say  that  such  green  prothallia  as  those  of  the  Marat- 
tiaceiE  and  Gleichenia,  which  contain  an  endophytic  fungus,  bear  somewhat  the 
same  relation  to  the  subterranean  prothallia  of  the  Ophioglossaceic  that  the  green 
Ericales  do  to  Monotropa. 

The  occurrence  of  a  similar  endophyte  has  also  been  noted  in  a  number  of 
liverworts.  Cavers  (Cavers  I)  has  studied  this  association  with  some  care  in  the 
common  liverwort,  Fegatella,  as  well  as  in  some  other  Hepatic;E.  He  found  in 
Fegatella  that  the  endophyte  is  beneficial  to  the  growth  of  the  host,  which  was  more 
vigorous  when  the  fungus  was  present.  He  assumed  that  this  was  due  to  the  assist- 
ance given  by  the  fungus  in  the  assimilation  of  organic  matter  from  humus  or  other 
organic  substrata.     (See  also  Humphrey  1). 

This  occurrence  of  an  endophyte  in  the  Hepatica-  makes  its  occurrence  in  the 
green  prothallia  of  ferns  readily  comprehensible.  Whether  in  the  latter  it  is  an 
advantage  to  the  host  to  have  the  endophyte  present  remains  to  be  seen,  but  it 
is  highly  probable  that  such  is  the  case.  Once  having  acquired  the  habit  of 
associating  itself  with  the  fungus,  the  gradual  evolution  of  the  purely  saprophytic 
subterranean  gametophyte  of  the  Ophioglossaceae  from  green  forms  similar  to  those 
of  the  Marattiace;e  is  readily  comprehensible. 


34 


THE    OPHIOGLOSSALES 


II.  THE  EMBRYO. 

The  development  of  the  embryo  in  the  Ophioglossaceae  has  been  more  or  less 
completely  studied  in  Ophtoglossum  pednnculosum,  O.  vulgatmu,  O.  moluccainim, 
O.  pendulum,  Botrychium  virgintaniim,  B.  liinarta,  and  B.  oblifjinini  (Mettenius  I, 
Bruchmann  1  and  2,  Lang  I,  Campbell  8,  Jeffrey  1,  Lyon  I). 

The  first  division  in  the  young  embryo  in  all  of  these  is  usually  approximately 
transverse,  although  there  may  be  a  good  deal  of  variation  in  this  respect.  It  is 
probable  that  in  all  cases  the  primary  root,  the  stem  ape.\,  and  the  foot  all  arise  from 
the  epibasal  region.  The  embryo  reaches  a  very  large  size  before  the  root  emerges 
from  the  overlying  prothallial  tissue  and  all  of  the  organs  of  the  young  sporophyte 
are  very  late  in  developing,  so  that  it  is  not  easy  to  trace  their  origin  back  to  the 
early  cell  divisions  in  the  young  embryo.  Much  the  most  conspicuous  organ  of  the 
young  sporophyte  is  the  root,  which  may  reach  a  very  large  size  and  an  advanced 
stage  of  development  before  any  evidence  of  the  other  organs  is  apparent.  Indeed, 
several  roots  may  be  developed  before  the  shoot  is  established.  In  Ophtoglossum 
vulgatum  and  Botrychium  lunarta,  according  to  Bruchmann's  account,  the  young 


Fig.  \%.—0[,hioglossum  ,r 

An  old  archegonium.      Xl8o. 
Two-celled  embryo  within  the  archegonii 
Two  sections  of  an  older  embryo.      Xl8< 


sporophyte  remains  several  years  under  ground  before  the  first  green  leaf  appears 
above  the  earth,  and  it  is  probable  that  in  Ophtoglossum  pendulum  there  is  also  a 
long  period  of  underground  existence  before  the  first  green  leaf  is  developed.  In 
Ophtoglossum  moluccanum,  however,  and  in  Botrychtum  virgintanum,  the  first 
leaf  developed  is  a  green  foliage  leaf,  which  grows  rapidly  and  soon  appears  above 
the  surface  of  the  ground. 

THE  EMBRYO  OF  OPHIOGLOSSUM. 

The  first  figures  that  we  have  of  the  embryo  of  Ophtoglossum  are  those  of 
Mettenius,  but  his  figures  of  the  embryo  of  O.  pedunculosum  are  not  at  all  satis- 
factory, although  he  shows  correctly  sections  of  the  older  sporophyte.  Lang  figures 
only  one  embryo,  a  somewhat  advanced  one  of  0.  pendulum.  Bruchmann  figures  a 
two-celled  stage  and  a  single  more  advanced  embryo  of  O.  vulgatum,  but  he  describes 
and  figures  several  stages  of  the  young  sporophyte.  My  own  study  of  Ophtoglossum 
was  based  mainly  upon  the  development  of  the  embryo  in  O.  pendulum,  where  a 


Tin-:   iMiuoo  35 

fairly  comjilcte  series  of  embryos  was  olnaiiud  and  rhr  (k\(lo|imtiir  lollowitl  quite 
satisfactorily. 

In  ().  rnohh,  iiiiiiin  1  foiiiul  two  <|iiirc  \oiin<i  cmhrNos,  rhr  \-oungest  consisting 
of  two  cells  (tig.  iS,  /?),  the  other  iiuich  more  advanced,  with  the  cotyledon  already 
differentiated  and  the  beginning  of  the  primary  root  recognizable.  In  the  first 
embryo  the  basal  wall  was  nearly  transverse  to  the  axis  of  the  archegonium  and,  to 
judge  from  the  arrangement  of  the  organs  of  the  older  embryo,  it  looks  as  if  the  whole 
of  the  hypobasal  region  formed  the  foot,  the  epibasal  half  giving  rise  to  the  cotyledon 
and  root,  ihe  older  embryo  (fig.  i8,  6')  was  cut  longitudinally  in  the  plane  of  the 
cotyledon,  which  at  this  time  comprises  pretty  much  the  whole  of  the  upper  part  of 
the  embryo,  the  hypobasal  region  being  occupied  mainly  by  large  cells  which  con- 
stitute the  foot.  Unfortunately,  in  this  series  the  section  containing  the  ape.x  of  the 
leaf  was  missing,  and  so  it  is  impossible  to  say  whether  at  this  stage  a  definite  apical 
cell  is  present  in  the  cotyledon;  but,  as  in  somewhat  older  stages  such  a  cell  seemed 
to  be  always  present,  it  is  probable  that  there  was  an  apical  cell  in  the  cotyledon  of 
the  embryo  in  question.  At  the  base  of  the  leaf,  and  almost  in  the  center  of  the 
embryo,  there  was  a  group  of  actively  growing  cells,  evidently  marking  the  position 
of  the  root  apex,  which  arises  deep  in  the  tissue  of  the  embryo,  very  much  as  we 
shall  see  to  be  the  case  in  the  Marattiaceae;  and  it  seems  probable  that  in  O.  tnoliic- 
canum,  as  in  Dancea,  the  root  grows  downward  through  the  foot  and  in  a  direction 
coincident  with  the  axis  of  the  young  cotyledon. 


19. — 0 phioglossum  vulgatum  (after  Bruchmai 


A.  Median  section  of  a  young  embryo.   Xi6o.    B.  An  older  embryo. 
C,  D.  Older  embryos,  showing  beginning  of  apical  bud,  i>;  r,  root.     X 


The  cotyledon  grows  upward  and  soon  ruptures  the  overlying  prothallial  tissue, 
while  the  root  grows  down  in  the  opposite  direction  and  pierces  the  prothallium  at  a 
point  some  distance  below  where  the  leaf  emerges.  As  the  root  grows  downward 
through  the  foot  the  latter  becomes  unrecognizable,  its  outer  cells  remaining, 
however,  as  a  zone  of  large  cells  encircling  the  equatorial  region  of  the  very  much 
elongated  bipolar  embryo. 

The  young  root  very  early  develops  a  tetrahedral  apical  cell,  like  that  of  the 
later  roots.  This  cell  is  probably  cut  out  from  the  central  tissue  of  the  embryo,  close 
to  the  base  of  the  leaf.  The  cell  r  in  fig.  18,  C,  to  judge  from  its  position  and  the 
arrangement  of  the  cells  around  it,  is  probably  the  initial  cell  of  the  primary  root. 

The  young  cotyledon  grows  rapidly  and  has  first  a  conical  form  (fig.  23,  B), 
terminating  in  a  definite  apical  cell.  As  it  grows  it  develops  a  small  oval  lamina 
and  a  slender  petiole,  and  presently  the  little  green  leaf  appears  above  the  surface 
of  the  earth. 

1  he  embr\o  of  ().  vulgatum  differs  remarkably  from  that  of  0.  mohiccanum  in 
the  late  development  of  the  leaf.  Bruchmann  was  unable  to  obtain  the  younger 
stages  of  the  embryo,  so  that  the  origin  of  the  different  members  is  still  somewhat 
obscure.     In  this  species  it  is  the  root  which  develops  first,  and  it  soon  becomes 


36 


THK    OPHIOGLOSSALES 


exceedingly  conspicuous.  Bruchmann  considers  that  the  root  and  toot  are  both  of 
hypobasal  origin,  but  he  bases  this  on  a  comparison  with  the  true  ferns  rather  than 
upon  actual  study  of  embryos,  as  he  was  unable  to  obtain  embryos  sufficiently  young 
to  demonstrate  this,  and  all  trace  of  the  original  divisions  disappears  before  any 
sign  of  the  stem  and  leaf  is  evident.  It  may  be  well  questioned  whether,  as  in 
Botrychium  and  0.  pendulum,  the  foot  does  not  take  up  the  whole  hypobasal  region. 
It  is  not  impossible  that  the  position  of  the  basal  wall  may  also  vary  in  O.  vulgatum. 
From  a  comparison  with  the  embryo  of  0.  pendulum,  I  am  inclined  to  assign  more 
of  the  embryo  of  the  former  to  the  foot  region  than  is  done  by  Bruchmann. 

In  O.  vulgatum  there  is,  finally,  a  differentiation  of  the  stem  apex  from  the 
epibasal  region,  as  in  Botrychium  and  the  true  ferns,  while  in  O.  moluecanum  there 
is  no  trace  of  a  stem  apex  in  the  very  young  sporophyte,  this  developing  later  as  a 
bud  upon  the  first  root. 

From  a  study  of  O phioglossum  moluccanum  and  also  ot  0.  pendulum  it  is 
evident  that  the  history  of  the  young  sporophyte  in  these  species  differs  strikingly 
from  that  of  the  other  Pteridophytes.  In  both  of  these  species  the  definitive  sporo- 
phyte always  arises  secondarily,  as  a  bud  upon  the  root,  in  the  same  way  that 
adventitious  buds  are  commonly  formed  upon  the  roots  of  the  adult  sporophyte. 
Bruchmann  notes  in  0.  vulgatum  the  very  precocious  development  of  the  primary 


A.  Transverse  section  of  very  young  embryo. 

B.  Longitudinal  section  of  young  embryo.     Xi8o. 

C.  Three  transverse  sections  of  an  older  embryo;   l-i,  basal  wall;  r,  primary  root.     XlSo. 
n.  An  older  embryo;  r,  primary  root. 

root  and  the  late  appearance  of  the  stem  apex  and  first  leaf;  but  in  this  species  the 
shoot  apex,  according  to  his  statement,  is  derived  directly  from  the  epibasal  half  of 
the  embryo,  as  it  is  in  most  Pteridophytes. 

In  Ophioglossum  pendulum,  where  the  development  of  the  embryo  seems  to 
offer  no  check  to  the  further  growth  of  the  prothallium,  the  position  of  the  arche- 
gonium  varies  a  good  deal  and  it  is  impossible  to  tell  from  a  section  just  what  the 
position  was  in  the  living  state,  as  the  branches  of  the  gametophyte  extend  in  all 
directions  and  archegonia  may  be  formed  at  any  point  upon  their  surface.  To 
judge  from  the  youngest  stages  of  the  embryo  that  were  met  with  (fig.  20),  the  basal 
wall  in  this  species  is  not  necessarily  transverse.  In  both  of  the  cases  figured  it 
was  oblique,  and  more  nearly  longitudinal  than  transverse.  It  is  likely,  however, 
that  it  is  horizontal,  or  approximately  so.  In  the  four-celled  embryo  shown  in 
fig.  20,  J,  the  quadrant  walls  were  at  right  angles  to  each  other,  and  this  was  also 
the  case  in  the  five-celled  embryo  shown  in  fig.  20,  B.  Somewhat  older  embryos  (C) 
show  that  there  is  a  pretty  regular  octant  formation,  and  Bruchmann  states  that 
this  is  also  the  case  in  O.  vulgatum. 

While  in  the  typical  ferns,  and  in  Botrychium,  all  of  the  organs  of  the  young 
sporophyte  can  be  traced  to  certain  regions  of  the  young  embryo,  in  Ophioglossum 


THK    KMHRVO  37 

pendulum  only  one  of  the  definitive  organs,  the  root,  arises  in  this  way,  and  this 
becomes  differentiated  at  a  very  early  period.  One  of  the  octants  next  to  the  arche- 
gonium  at  once  becomes  the  apical  cell  of  the  young  root.  This  cell  is  very  soon 
recognizable  by  its  size  and  shape,  and  quickly  begins  its  regular  segmentation. 
The  primary  cap-cell  is  soon  cut  off  (fig.  20,  D),  and  from  now  on  the  young  root 
is  very  conspicuous.  The  octant  divisions  are  vc-ry  clearly  marked  in  this  case, 
and  in  section  3,  which  is  the  uppermost  of  the  three,  the  large  triangular  apical 
cell  of  the  root  is  very  evident. 

Two  types  of  the  embryo  were  seen  in  this  species.  One  ot  these  (fig.  21,  A) 
is  nearly  globular  in  form;  the  other  (fig.  21,  /i,  6")  is  elongated.  The  former  looks 
as  if  it  originated  from  an  embryo  in  which  the  basal  wall  was  transverse  to  the  a.\is 
of  the  archegonium;  in  the  other  it  was  probably  more  or  less  vertical.  It  is  probable 
that  in  the  former  instance  the  root  initial  is  one  of  the  epibasal  octants,  while  the 
whole  of  the  hypobasal  portion  gives  rise  to  the  large  foot.  In  the  second  type  it  is 
difficult  to  say  which  half  should  be  considered  epibasal  and  which  h\p()basal,  hut, 
as  in  the  other  case,  one  half  ma\'  be  considered  to  be  root,  thc'  other  halt  tout,  the 


C.  Older  embryo,  with  single  root. 

D.  Embryo  with  two  roots;   /)r,  gametopliyte.    Shaded  region  occupied  bv  the  mycorrhir.a. 

growth  of  both  being  nearly  in  a  plane  at  right  angles  to  that  of  the  archegonium 
axis,  andl  suggesting  the  relative  positions  of  cotyledon  and  foot  in  the  embr}o  of 
Ophioglossum  moluccanum. 

In  form  the  first  type  somewhat  recalls  the  embryo  of  Boirychium  virginianum. 
The  whole  lower  portion,  or  hypobasal  half,  forms  the  very  conspicuous  foot,  while 
from  the  epibasal  region  the  primary  root  is  developing,  and  already  the  rudiment 
of  the  second  root  is  visible.  Whether  the  latter  arises  directly  from  the  primary 
root,  or  whether  it  arises  independently  from  the  second  epibasal  quadrant,  is  not 
quite  certain.  The  cells  of  the  epibasal  region  are  evidently  actively  growing,  having 
abundant  protoplasm  and  conspicuous  nuclei.  The  cells  of  the  foot  are  larger  and 
much  more  transparent. 

The  second  type  of  embryo  (fig.  21,  B,  C)  resembles  very  closely  the  second 
state  of  the  embrxo  of  Opinocrlossinn  viilguturii,  where,  as  is  said  b\'  Hruchinaiin, 
rlu-  embr\()  is  "all  root." 


38 


THE    OPHIOGLOSSALES 


In  O.  molticcanuni  the  prothallium  probably  lives  for  a  single  season  only,  and 
the  formation  of  the  sporophyte  stops  its  further  development;  but  in  0.  pendulum, 
where  embryos  are  much  less  frequently  found,  the  large  gametophyte  continues 
its  growth  apparently  unchecked  by  the  development  of  the  attached  sporophyte, 
which  retains  its  connection  with  the  gametophyte  for  a  very  long  time,  as  in  0. 
vulgatum  and  Botrychium  virgmianum. 

The  embryo  reaches  a  very  large  size  before  it  breaks  through  the  prothallium. 
The  primary  root  then  emerges  as  a  conical  point  (fig.  3,  F,  sp).  The  second  root 
remains  short  for  a  time.  There  seems  to  be  a  good  deal  of  difference  as  to  the  time 
of  the  appearance  of  the  latter.  In  the  globular  type  of  embryo  the  second  root 
appears  very  early,  and  it  looks  as  if  it  might  have  been  formed  quite  independently 
of  the  primary  root.  Sometimes,  however,  the  primary  root  may  attain  a  length  of 
several  centimeters,  and  may  even  begin  to  form  rootlets  before  the  second  root 
emerges;  while  in  other  cases  the  two  roots  grow  in  opposite  directions  and  seem  to 
be  of  about  equal  size  (fig.  3,  E). 

The  leafy  shoot  in  Ophioglossum  pendulum 
does  not  appear  until  the  root  system  is  well 
advanced.  The  primary  root,  although  attaining 
a  length  of  10  centimeters  or  more,  in  no  cases 
showed  any  signs  of  leaf-bearing  buds  in  the 
specimens  that  I  collected.  Rootlets  were  devel- 
oped in  some  cases,  and  it  is  not  impossible  that 
there  may  be  an  extensive  development  of  the 
root  system  before  the  first  leafy  bud  is  formed. 
This  is  quite  in  harmony  with  the  large  develop- 
ment of  the  roots  in  O.  vtilgatum,  where  Bruch- 
mann  believes  that  it  may  be  eight  or  ten  years 
before  the  first  foliage  leaf  appears  above  the 
ground.  In  O.  vulgatum,  however,  this  leaf  arises 
from  the  original  stem  apex  derived  directly  from 
the  embryo,  and  not  from  an  adventitious  bud. 
Ophioglossum  moluccanum  and  the  similar 
species  that  grow  with  it  differ  very  much  from 
Ophioglossum  pendulum  in  the  character  of  the 
young  sporophyte,  which,  as  we  have  seen,  at  once 
develops  a  green  foliage  leaf  or  cotyledon.  The 
sporophyte  very  closely  resembles  that  of  O. /jf  </;//;- 
culosum  described  by  Mettenius;  in  fact,  the 
resemblance  is  so  close  that  it  would  seem  to 
confirm  the  close  relationship  of  this  species  and 
""*■  possibly  its  identity  with  some  of  the  forms  asso- 

ciated by  Raciborski  under  the  name  0.  moluccanum  (Raciborski  I). 

As  Mettenius  correctly  showed  in  O.  pedunculosum,  the  first  organ  to  be 
developed  is  the  cotyledon,  which  soon  pierces  the  earth  and  appears  as  a  green 
foliage  leaf  This  primary  leaf  is  continued  directly  into  the  primary  root,  but  no 
stem  apex  is  developed,  nor  is  any  sheath  formed  about  the  leaf  base  in  the  young 
sporophyte,  which  consists  practically  of  leaf  and  root  alone.  The  latter  often 
penetrates  for  some  distance  into  the  prothallial  tissue  before  it  emerges,  so  that  the 
central  portion  of  the  young  sporophyte  is  surrounded  by  a  sheath  formed  by  the 
prothallial  tissue.  A  longitudinal  section  of  the  sporophyte  (fig.  22,  A)  shows  that 
the  tissues  of  the  leaf  are  continued  directly  into  those  of  the  primary  root.     A 


Fig.  11.— Ophioglossum  moluccanum. 

A.  Median    section  of   young  sporophyte    before 

formation    of    bud;    /,   cotyledon;     r,   root, 
pr,  the  gametophyte.     X15. 

B.  Central  region  of  same,  more  enlarged;    /r, 

first  tracheids. 

C.  An    older   sporophyte,    showing    bud,   fc,    de- 

veloping from  primary  root.     X15. 

D.  E.  Lamina   of  cotyledon,  showing  venation. 


THE    EMBRYO 


39 


single  axial  vascular  bundle  traverses  the  whole  of  the  young  sporophyte  without 
interruption,  and  there  is  no  recognizable  boundary  between  the  tissues  of  the  leaf 
base  and  those  of  the  root.  The  central  region  of  the  embryo  is  somewhat  thickei 
and  its  outer  cells  are  enlarged,  these  outer  cells  probably  belonging  to  the  foot 
through  which  the  root  has  penetrated  and  which  at  this  period  can  not  be  clearly 
recognized.  The  strictly  bipolar  character  of  the  young  sporophyte  and  the  way 
in  which  it  perforates  the  gametophyte  resemble  most  nearly  the  corresponding 
stages  of  Equisetum  and  the  Marattiace;e,  and  it  may  be  said  that  Lyon's  recent 
studies  on  Botrychium  ohli(juum  indicate  that  in  this  species  also  there  is  a  similar 
bipolar  arrangement  of  leaf  and  root. 

Mettenius  pointed  out  in  O.  pedunculosum  that  the  definitive  sporophyte  arises 
as  an  adventitious  bud  upon  the  primary  root,  either  close  to  the  leaf  base  or,  more 
commonly,  at  some  distance  from  it.  This  is  also  the  case  in  O.  nioluccanum  and 
the  other  allied  species.  In  one  case  observed  by  me  two  independent  sporophytes 
were  found  growing  from  the  same  prothallium,  but  this  is  unusual,  and  in  most  of 
the  cases  where  two  sporophytes  seem  to  be  present,  one  of  these  is  realh'  the  sec- 
ondary sporophyte  growing  from  the  primary  root. 


Fig.  23. — Ophioglosium  moluccanum. 

A.  Young  cotyledon,  longitudinal  section;  /)r,  gametophyte.     x8o. 

B.  Apex  of  cotyledon  more  highly  magnified;  x,  apical  cell. 

C.  Young  sporophyte  in  which  a  rudimentary  second  leaf  (/")  is  present.   XSo. 

D.  Cross-section  of  apex  of  primary  root.     X200. 

While  in  O.  vidgatum  the  sporophyte  stays  under  ground  for  several  years, 
in  O.  moluccanum  there  is  every  reason  to  believe  that  there  is  only  a  brief  interval 
between  the  first  formation  of  the  leaf  and  its  appearance  above  ground.  The  small 
size  and  the  character  of  the  gametophyte,  as  well  as  the  quick  germination  of  the 
spores  and  the  rapid  growth  natural  to  a  tropical  climate,  indicate  that  the  gameto- 
phyte is  an  annual  and  that  it  dies  as  soon  as  the  young  sporophyte  is  established. 

In  0.  pendulum  the  primary  root  as  it  breaks  through  the  prothallium  elongates 
rapidly,  but  just  how  far  it  grows  before  the  bud  is  formed  upon  it  could  not  be 
determined.  These  roots  are  very  brittle  and  easily  broken  off,  and  in  no  cases  were 
young  buds  found  upon  roots  which  were  still  connected  with  the  prothallium.  The 
first  root  sometimes  reaches  a  length  of  3  or  4  centimeters  before  the  second  root  can 
be  seen  at  all.  The  growth  of  the  roots  in  the  young  sporophyte  is  in  all  respects 
like  that  occurring  in  the  older  ones.  There  is  a  large  tctrahcdral  apical  cell,  the 
divisions  ot  which  are  quite  regular,  and  the  conspicuous  axial  vascular  cyliiuK  1  is 


40  THE    OPHIOGLOSSALES 

developed  at  an  early  period.  The  stele  of  the  second  root  joins  that  of  the  first 
where  the  latter  joins  the  foot  (fig.  21,  D).  The  primary  root  in  O.  pendulum  is, 
usually  at  least,  diarch. 

DEVELOPMENT  OF  THE  PRIMARY  BUD  IN  OPHIOGLOSSUM  MOLUCCANUM. 

The  several  terrestrial  species  of  Ophioglossum  growing  at  Buitenzorg  and 
associated  under  the  name  O.  moluccanum  differ  strikingly  from  O.  vulgatum  in  the 
further  history  of  the  young  sporophyte  as  well  as  in  the  early  development  of  the 
first  functional  leaf.  This  difference  is  also  found  in  the  young  sporophyte  of  O. 
reticulatum  ( t)  collected  at  Hakgala  in  Ceylon.  All  of  these  tropical  species  agree 
with  O.  pedunculosum,  which  was  correctly  described  by  Mettenius  (Mettenius  1), 
in  the  origin  of  the  definitive  axis  which  arises  as  an  adventitious  bud  from  the 
primary  root  of  the  young  sporophyte.  A  similar  condition  of  things  probably  is 
true  also  in  O.  pendulum,  although  in  the  latter  no  leaf  is  at  first  developed  from  the 
young  sporophyte,  which  is  composed  exclusively  of  one  or  two  roots  in  addition  to 
the  foot,  so  that  the  first  leaf  in  O.  pendulum  is  also  an  adventitious  structure. 
Whether  or  not  the  primary  leaf  in  0.  pendulum,  and  probably  at  the  same  time  the 
stem  apex,  arises  as  a  bud  from  the  primary  root,  or  whether  (which  seems  more 
likely)  it  is  developed  from  a  secondary  root,  can  not  be  stated,  as  no  young  leafy 
buds  were  found  in  connection  with  the  gametophyte. 


Fig.  24. — Ophioglossum  moluccanum, 

A.  Tangential  section  of  primary  root,  showing  young,  endogenous  bud,  b.    X  about  50. 

B.  C.  Two  sections  of  tfie  same  bud.    B,  tfie  first  leaf;  C,  stem  apex.     X150. 

D.  Two  transverse  sections  of  a  young  bud;   l  passes  through  stem  apex  st;  2,  through  leaf. 

Mettenius  gives  no  detailed  study  of  the  development  of  the  bud  upon  the  root, 
nor  does  he  state  whether  he  recognized  its  endogenous  origin.  The  bud  arises 
much  in  the  same  way  that  a  secondary  root  does,  and  is  not  visible  upon  the  out- 
side of  the  root  until  it  is  far  advanced  in  its  development,  the  young  leaf  breaking 
through  the  overlying  tissues  in  much  the  same  way  that  a  young  root  emerges.  In 
two  instances  the  rudiment  of  the  young  bud  could  be  seen  close  to  the  apical 
meristem  of  the  root,  in  a  position  which  is  exactly  the  same  as  that  described  for  the 
leafy  buds  formed  at  the  apex  of  the  root  in  O.  vulgatum.  More  commonly,  the 
bud  originated  nearer  the  base  of  the  root,  but  it  may  arise  at  any  point  between 
the  base  and  the  apex.  Figure  24  shows  sections  of  the  youngest  buds  that  were 
found.  //  is  a  tangential  section  of  the  primary  root,  in  which  the  young  bud  has 
formed  at  a  point  not  very  far  back  from  the  root  apex,  r.     The  first  leaf  of  the  young 


THE    FMHRVO 


41 


hml  aiul  tlu-  young  stem  :ipt\  can  alix'acl\-  Ik-  iccogni/A-il,  and  tlit-se  lia\c  appaic-ntly 
developed  quite  independently  of  each  other.  Fhe  leaf  rudiment,  B,  lies  nearer  the 
bundle  of  the  main  root  and  may  perhaps  have  taken  its  origin  from  a  single  endo- 
dermal  cell,  but  this  could  not  be  certainly  determined.  The  young  leaf  soon  forms 
a  slightly  projecting  conical  body,  composed  of  a  few  cells  with  conspicuous  nuclei, 
separated  from  the  adjacent  root  tissue  by  a  small;|space.  At  this  stage  it  is  not  quite 
clear  whether  the  apical  cell  has  been  developed,  but  later  stages  show  the  presence 
of  an  unmistakable  apical  cell  of  approximately  tetrahedral  form.  Lying  nearer 
the  periphery  of  the  root  is  the  young  stem  ape.x,  composed  of  a  small  group  of 
meristematic  cells,  one  of  which  is  unmistakably  the  initial  cell  for  the  stem.  This 
apical  cell  is  truncate  below  and  the  base  is  broader  than  the  outer  free  face.  Above 
the  stem  apex  can  be  seen  the  cavity  which  separates  the  outer  tissues  of  the  young 
bud  from  the  cortical  tissue  of  the  root. 

Fig.  24,  D,  shows  two  transverse  sections  of  a  but!  of  about  the  same  age  as  the 
one  just  described.  No.  i  passes  through  the  stem  apex  and  shows  the  conspicuous 
triangular  apical  cell;  No.  2  shows  a  section  of  the  leaf  above  the  level  of  the  stem 
apex  with  the  basal  tissue  of  the  leaf  extending  around  the  stem  region.  This  is  the 
beginning  of  the  hollow  stipular  sheath  which  incloses  the  stem  apex  of  the  bud  and 


A.  Bud  about 

B.  Apex  of  le; 


)  break  through  primary  root; 
more  highly  magnified. 
Transverse  section  of  a  young  bud  passing 

D.  Section  of  same  passing  through  stem  apex,  .v. 

E.  Transverse  section  of  stem  apex  from  an  older  sporophyt 


stem  apex.    X  about  80. 
gh  base  of  leaf,  /.     X 1 50. 

The  apical  cell  is  four-side 


which  is  so  conspicuous  a  feature  in  the  stem  apex  of  the  older  sporophyte.  Probably 
the  large  central  cell  in  the  section  of  the  leaf  shown  in  No.  2  is  the  apical  cell,  but 
this  is  not  quite  certain. 

A  transverse  section  of  a  somewhat  older  bud  (fig.  25,  C)  shows  a  nariow  cleft 
at  the  base  of  the  leaf  in  front,  opening  into  a  cavity  within  which  the  stem  apex  lies. 
It  is  impossible  to  say  exactly  how  much  of  this  stipular  sheath  really  belongs  to  the 
leaf  base  and  how  much  is  derived  directly  from  the  adjacent  cortical  tissue  of  the 
root,  since  the  tissues  of  the  leaf  base  merge  insensibly  into  the  latter.  From  this 
time  on,  each  new  leaf  develops  this  conical  stipular  sheath,  which  incloses  the  stem 
apex  and  the  next  youngest  leaf,  and  which  has  so  ofttn  Ikiii  discrihcd  in  the  oUKr 
sporophyte. 

If  a  median  section  of  the  young  bud  is  examined  just  before  the  bud  breaks 
through  the  overlying  tissues  of  the  root  (fig.  25,  A),  it  can  be  clearly  seen  that  the 
leaf,  which  now  has  the  form  of  an  elongated  cone,  lies  above  the  level  of  the  young 
stem  apex,  and  by  this  time  the  differentiation  of  the  vascular  bundle  of  fhe  leaf  is 
well  advanced.    This  bimdle  connects  with  the  vascular  bimdle  of  the  primary  root 


42  THE    OPHIOGLOSSALES 

and  there  is  no  connection  between  it  and  the  tissues  of  the  stem  apex  of  the  bud. 
The  latter  consists  of  a  shallow  mass  of  tissue  with  the  conspicuous  apical  cell  in 
the  center,  but  below  it  there  is  no  sign  of  the  development  of  any  procambium. 
The  stem  apex  lies  in  a  depression  formed  by  a  shallow  ridge,  which  encircles  it 
and  forms  the  beginning  of  the  stipular  sheath  belonging  to  the  base  of  the  leaf. 
The  exact  limits  of  the  basal  tissue  of  the  leaf,  as  we  have  already  stated,  can  not 
be  clearly  defined.  The  cavity  above  the  stem  apex  is  still  very  evident,  but  how 
much  of  the  tissue  lying  above  the  cavity  belongs  to  the  leaf  base,  and  how  much  to 
the  cortical  tissue,  is  not  clear.  The  section  through  the  apex  of  the  leaf  (fig.  25,  B) 
shows  a  single  large  terminal  cell  which,  without  doubt,  is  the  apical  cell. 

The  young  bud  is  now  ready  to  emerge  and,  very  soon  after,  the  rapidly  elongat- 
ing apex  of  the  young  leaf  pushes  through  the  outer  root  tissue  and  emerges  upon 
the  outside.  The  stem  apex  remains  buried  within  the  root  tissues  and  the  sheathing 
base  of  the  leaf.  The  leaf  base  is  surrounded  by  a  ragged  sheath,  formed  by  the 
ruptured  outer  tissues  of  the  root. 

The  development  of  the  bud  upon  the  root  in  O.  pendulum  unfortunately  could 
not  be  followed.  The  smallest  leaves  found  were  10  centimeters  or  more  in  length, 
and,  although  these  were  probably  the  primary  leaves,  they  were  not  recognized  as 
such  at  the  time  the  plants  were  collected,  and  so  there  was  no  opportunity  of  tracing 
their  connection  with  the  original  root. 

The  fully  developed  cotyledon  in  what  may  be  considered  the  typical  form  of 
O.  moluccaniim  is  more  or  less  lanceolate  in  outline  (fig.  22,  D).  There  is  a  central 
vein  from  which  branch  secondary  veins  on  either  side,  connecting  with  the  central 
vein  by  anastomosing  branches  which  inclose  elongated  meshes.  In  the  form  with 
broader  leaves,  probably  another  species,  the  mid-vein  is  more  obscure  and  the 
meshes  are  broader  and  more  numerous. 

Three  types  of  the  embryo  may  be  recognized  in  Ophioglossum,  represented 
respectively  by  O.  mohiccaiium,  O.  vulgatum,  and  O.  pendulum.  If,  as  seems  not 
unlikely,  O.  moluccanum  is  the  most  primitive  of  the  three,  some  interesting  points 
arise  as  to  the  significance  of  the  peculiarities  exhibited  by  the  embryo,  which  shows 
only  two  organs  aside  from  the  foot,  viz,  the  cotyledon  and  primary  root,  these 
growing  in  an  almost  exactly  opposite  direction,  without  any  clear  line  of  demarca- 
tion between  them.  I  have  ventured  to  draw  a  comparison  between  the  sporophyte 
of  Ophioglossum  and  that  of  Anthoceros,  assuming  that  the  former  has  arisen  from 
some  bryophytic  type  not  unlike  Anthoceros,  by  the  development  of  a  root  from  the 
base  of  the  sporogonium  and  of  a  special  foliar  organ  from  the  basal  meristem  of 
such  a  sporogonium.  The  embryo  of  0.  moluccanum  approaches  this  hypothetical 
form,  as  it  consists  only  of  leaf  and  root,  and  no  stem  apex  is  developed  from  it, 
its  growth  being  of  limited  duration.  In  this  case  the  definitive  sporophyte  is  a 
secondary  structure  developed  as  a  bud  upon  the  primary  root.  In  O.  vulgatum, 
however,  the  definitive  stem  apex,  although  of  very  late  origin,  is  apparently  a 
product  of  the  original  embryonic  tissue,  but  the  first  foliage  leaf  is  of  much  later 
origin.  In  0.  pendulum  the  formation  of  the  leafy  sporophyte  is  also  secondary, 
but  neither  stem  apex  nor  leaf  is  developed  from  the  embryo  itself. 

If,  as  the  writer  believes,  Ophioglossum  represents  the  most  primitive  type  of 
the  fern  series,  it  is  quite  conceivable  that  in  O.  moluccanum  and  its  allies  the  embryo 
represents  the  condition  existing  in  the  ancestral  type  from  which  these  have  sprung. 
On  the  supposition  that  the  leafy  sporophyte  is  derived  from  a  large  bryophytic 
sporogonium  resembling  that  oi  Anthoceros,  there  must  have  been  a  stage  when  the 
sporophyte  consisted  of  two  parts  only,  the  upper  sporogenous  portion,  which  later 
developed  into  a  sporophyll,  as  represented  in  Ophioglossum,  and  the  root.     Of 


THE    EMBRYO  43 

course,  it  is  quite  possible  that  the  pecuhar  origin  of  the  detinitive  sporophyte  in 
O.  moluccanum  and  O.  pedunculosiim  is  secondary,  but  this  is  by  no  means  neces- 
sarily the  case.  However,  it  seems  highly  probable  that  the  extraordinary  develop- 
ment of  the  roots  in  O.  vulgatuni  and  O.  prmiuliim  and  the  protracted  subterranean 
life  in  these  species  constitute  a  secondary  phenomenon  associated  with  the  pro- 
nounced saprophytic  life  of  the  gametophyte. 

The  apex  of  the  shoot  lies  in  a  narrow  depression  between  the  base  of  the  leaf 
and  a  narrow  ridge  which  extends  around  it  on  the  side  opposite  the'leaf  base.  This 
ridge  is  the  beginning  of  the  conical  sheath  characteristic  of  the  shoot  apex  of  the 
older  spf)rophyte.  A  transverse  section  of  the  young  apex  at  about  this  time  shows 
that  the  apical  cell  is  triangular  in  outline. 

The  first  root  of  the  young  bud  does  not  emerge  until  the  leaf  is  nearly  complete. 
From  this  time  on  the  further  growth  is  due  to  the  activity  of  the  stem  apex,  from 
which  new  leaves  and  rt)ots  presumably  are  developed  in  the  same  way  as  in  other 
species  that  have  been  studied.  How  long  it  is  before  fertile  leaves  are  formed  was 
not  ascertained,  but  in  the  rapidly  growing  species  of  a  tropical  climate  it  is  likely 
that  this  takes  place  before  long.  The  occurrence  of  very  small  fertile  individuals 
(fig.  55,  B)  points  to  this. 

THK  KMBRYO  OF  OPHIOGLOSSUM  VULGA'lUM. 

The  embryo  of  O.  vulgatuni  (Bruchmann  1)  differs  from  that  of  both  O. 
pendulum  and  O.  moluccanum  in  its  development,  but  in  the  earlier  stages  it  closely 
resembles  the  former  species.  As  in  O.  pendulum,  the  root  is  the  first  organ  to  be 
developed  and  it  reaches  a  large  size  before  there  is  any  indication  of  the  formation 
of  a  stem  apex  or  cotyledon.  Bruchmann  states  that  the  root  apex  arises  from  the 
hypobasal  half  of  the  embryo,  but  his  figure  (fig.  19,  A)  of  the  young  embryo,  where 
the  root  apex  is  just  visible,  closely  resembles  a  corresponding  stage  in  O.  pendulum, 
where  the  root  is  certainly  of  epibasal  origin;  and,  to  judge  from  the  elongated  form 
of  the  two-celled  embryo  which  Bruchmann  figures,  one  is  inclined  to  believe  that 
the  basal  wall  is  really  at  right  angles  to  the  long  axis  of  tlie  embryo,  and  not  parallel 
with  it,  as  l>e  figures,  so  that  the  whole  of  the  hypobasal  part  might  be  interpreted 
as  the  foot,  while  the  root  would  be  of  epibasal  origin,  as  it  is  in  O.  pendulum. 

The  next  stage  figured  by  Bruchmann  (fig.  19,  B)  is  very  much  like  the  type  of 
0.  pendulum,  where  only  one  root  was  developed  at  first,  and  in  this  case  also  we  are 
inclined  to  consider  the  whole  of  the  enlarged  base  ot  the  embryo  as  the  foot. 

Before  the  cotyledon  and  stem  apex  can  be  recognized  the  first  tracheary  tissue 
of  the  root  has  already  been  developed,  and  about  the  same  time  the  apex  of  the 
second  root  can  be  seen  arising  near  the  base  of  the  primary  root  (fig.  19,  C). 

The  cotleydon  arises  near  the  base  of  the  root,  upon  the  upper  side  of  the 
embryo,  and  forms  a  small  conical  protuberance,  which  grows  from  a  definite  apical 
cell.  At  the  base  of  the  cotyledon,  on  the  side  turned  away  from  the  root  apex,  a 
shallow  depression  is  formed,  and  in  this  there  may  be  seen  a  single  large  superficial 
cell,  which  is  apparently  the  apical  cell  of  the  very  limited  stem  apex.  Inclosing  the 
cotyledon  and  the  stem  apex  is  an  elevated  ridge  which  grows  up  about  them  and 
finally  forms  a  sheath,  which  rapidly  grows  so  as  to  include  the  bud  within  a  cavity 
completely  closed  except  for  a  narrow  canal  which  opens  outward. 

While  the  cotyledon  and  stem  apex  are  thus  formed  from  superficial  tissue  in 
().  vulgatuni,  their  early  inclosure  in  the  sheath  suggests  that  we  have  to  do  with  a 
condition  intermediate  between  the  completely  endogenous  shoot  apex  in  O.  moluc- 
canum and  the  entirely  exogenous  shoot  in  Butrychtum. 


44 


THE    OPHIOGLOSSALES 


The  second  root  arises  quite  independently  of  the  stem  apex,  being  developed 
below  the  insertion  of  the  primary  root,  and  its  vascular  bundle  joins  that  of  the 
first  root  near  its  base. 

A  rudimentary  vascular  bundle  is  developed  within  the  cotyledon,  and  also 
joins  the  bundle  of  the  main  root  near  its  base,  but  no  bundle  at  all  is  developed 
within  the  stem.  The  cotyledon  reaches  only  a  very  small  size,  but  the  second  leaf 
soon  appears  nearly  opposite  the  cotyledon. 

The  second  leaf  also  develops  at  an  early  period  a  vascular  bundle,  which 
connects  with  the  vascular  bundle  of  the  primary  root  near  its  point  of  junction  with 
the  second  root,  and  this  exactly  resembles  the  arrangement  of  the  bundles  in  the 
bud  formed  upon  the  root  in  O.  moluccanum.  It  is  evident  that  in  the  young  sporo- 
phyte  of  O.  viilgatuni,  as  in  O.  moluccanum,  the  vascular  system  is  made  up  entirely 
of  the  bundles  of  the  roots  and  leaves,  the  stem  itself  having  no  proper  stele. 

The  second  leaf  finally  emerges  and  appears  above  ground  as  the  first  sterile 
green  leaf  of  the  young  sporophyte.  Bruchmann  states  that  the  second  leaf  does  not 
appear  above  ground  until  five  years  after  it  is  first  formed,  and  he  believes  that  the 
sporophyte,  at  the  time  its  first  leaf  appears  above  ground,  is  nine  to  ten  years  of  age. 

The  third  leal  may  be  fertile,  but  this  is  not  always  the  case. 

THE  ANATOMY  OF  THE  YOUNG  SPOROPHYTE  OF  OPHIOGLOSSUM. 

In  Ophtoglossum  pendulum  the  young  primary  root  soon  breaks  through  the 
prothallium  and  elongates  rapidly,  but  owing  to  its  brittleness  it  is  easily  broken 
off,  and  it  is  impossible  to  state  here  just  how  far  it  develops  before  the  bud  is 
formed  upon  it.  The  development  of  the  second  root  varies  a  good  deal.  The  first 
root  may  reach  a  length  of  3  or  4  centimeters  before  the  second  root  can  be  seen 
at  all.  The  growth  of  these  earlier  roots  is  in  all  respects  similar  to  that  of  the  later 
ones.     There  is  a  large  tetrahedral  apical  cell  whose  divisions  are  quite  regular, 

and  there  is  soon  visible  the  axial  vascular 
bundle  which  extends  for  some  distance 
into  the  foot,  where  it  ends  blindly.  The 
vascular  bundle  of  the  second  root  joins 
the  first  at  the  junction  of  the  latter  with 
the  foot  (fig.  21,  D). 

The  first  tracheary  tissue  appears  at 
the  point  of  junction,  and  is  made  up  of 
short,  somewhat  irregular,  pointed  tra- 
cheids  with  reticulate  thickenings.  From 
this  point  the  development  of  the  tracheary 
tissue  proceeds  toward  the  apex  of  the  roots. 
The  bundle  is  diarch,  as  is  plainly  seen  in 
cross-sections  (fig.  27,  E').  The  endodermis 
is  very  clearly  defined  and  the  characteristic 
radial  markings  are  extraordinarily  clear, 
especially  in  sections  treated  with  a  double 
stain  of  safranine  and  gentian  violet.  The 
tracheary  tissue  is  also  beautifully  differen- 
tiated by  this  stain.  The  bundle  is  slightly 
elliptical  in  form  and  the  protoxylem  ele- 
ments appear  at  the  foci  of  the  elliptical 
section.  1  he  first  appearance  of  the  tracheary  tissue  is  some  distance  back  of  the 
apex  and  the  development  proceeds  rather  slowly.     In  the  oldest  part  of  the  roots 


older  bud   of    Ophiogh. 
of  the   bud. 


THK    I;MI!KV() 


45 


exaniiiud  rlic  tun  wlcm  masses  wcic  iiiU(|Lial  in  si/.r,  tin-  lai<ii-i  showing  ahmit 
half  a  dozen  tiacheids  in  cross-section,  the  smallei  two  or  three.  Whether  the  two 
protoxylems  are  uhimately  joined  hy  intermediate  tracheal  tissue,  so  as  to  form  a 
continuous  plate,  as  in  the  older  roots  of  the  adult  plant,  can  not  now  be  stated,  hut 
in  no  cases  examined  was  this  true,  and  it  is  not  unlikely  that  in  the  primary  root 
the  two  xylem  masses  are  permanently  separated.  The  cells  of  the  foot,  as  usual, 
are  more  or  less  papillate  where  they  are  in  contact  with  the  tissue  of  the  gameto- 
phyte.  They  early  become  infected  with  the  endophyte,  which  probably  makes  its 
entrance  from  the  prothallial  tissue,  and  not  from  the  outside.  i"his  point,  however, 
is  not  perfectly  clear.  The  infected  area  follows  the  giowtli  of  the  young  root,  but 
leaves  the  apical  tissues  tree. 

in  ().  moluccanum  the  leaf  is  the  Hrst  part  of  the  young  sporophyte  to  develop. 
In  the  larger  embryos  the  leaf  forms  a  conical  body,  merging  into  a  nearly  globular 
basal  portion,  which  is  the  foot,  and  within  this,'  probably  near  the  junction  of  the 
epibasal  and  hypobasal  halves  of  the  embryo,  the  apical  cell  of  the  root  is  developed. 
The  leaf  now  shows  a  definite  apical  cell,  triangular  in  .section  and  exhibiting  a 
regular  segmentation.  The  inner  cells  of  the  segments  form  the  axial  strand  of 
tissue,  which  is  continued  through  the  embryo  into  the  root.     1  he  limits  of  the  two 


Section  of  petiole  of  tcttyledon  o 
Section  of  young  root. 
Vascular  bundle  of  median  regie 
Vascular  bundle  of  primary  root 


of  O.  pcn.lulu 


primary  organs,  the  leaf  and  the  root,  remain  quite  indistinguishable.  The  central 
region,  which  remains  surrounded  by  the  prothallial  tissue,  is  somewhat  larger  in 
diatneter  and  the  whole  of  this  functions  as  a  foot,  although  it  is  composed  in  part 
of  tissue  belonging  to  the  root  and  the  leaf.  The  young  leaf  elongates  rapidly  after 
it  has  ruptured  the  calyptra,  and  its  apex  begins  to  widen  out,  but  still  shows  a 
single  apical  cell.  As  the  upper  part  widens  out  there  is  a  division  of  the  original 
vascular  cylindci,  and  there  is  developed  within  the  leaf  a  reticulate  s\stcm  of 
vascular  bundles  or  veins  (fig.  22.  D,  E). 

As  already  indicated,  the  vascular  stranil  of  the  \(iung  spoioplnte  is  continuous 
through  the  cotyledon  and  root,  and  sections  at  difttrent  points  show  essentially  the 
same  structure.  The  petiole  of  the  cotyledon  (fig.  27,  A),  which  is  traversed  by  two 
large  lacuna,  shows  that  the  axial  bundle  is  decidedly  collateral  in  structure.  The 
xylem  consists  of  a  group  of  about  half  a  dozen  tiacheids  at  the  inner  limit  of  the 
bundle,  and  no  endodermis  can  be  recognized.    As  a  section  of  the  bundle  is  made 


46  THK    OPHIOGLOSSALES 

in  the  mid-region  of  the  sporoph}te  (fig.  27,  C),  the  only  ditterence  noted  is  a  slightly 
greater  development  of  the  xylem.  The  section  of  the  root  (fig.  27,  D)  presents 
almost  exactly  the  same  appearance  as  that  of  the  leaf.  Whether  we  should  call  the 
root  bundle  "monarch"  or  "collateral"  is  merely  a  question  of  terms.  In  the  mid- 
region  the  endodermis  can  be  clearly  seen,  and  it  is  then  evident  that  the  xylem  is 
separated  from  it  by  a  single  layer  of  pericycle  cells. 


I  of  Botrychium  virginianumj  containing  a  two-celled  embryo 
B.  Four  longitudinal  sections  of  an  embryo  with  7  cells.     X275. 


THE  EMBRYO  OF  BOTRYCHIUM. 

The  following  account  of  the  development  of  the  embryo  of  Botrychium  is 
based  mainly  upon  material  of  B.  virginianiim  furnished  me  through  the  kindness 
of  Professor  Jeffrey. 

In  this  species,  as  in  the  other  Eusporangiatae,  there  is  a  marked  increase  in  the 
size  of  the  fertilized  ovum  before  the  first  division  takes  place.     At  the  time  of  the 


nbryos  of  Botrychi 


first  division  the  ovum  is  generally  more  or  less  elongated,  but  this  is  not  always  the 
case.  This  elongation  is  less  marked  in  B.  hinaria  (fig.  36),  while  in  B.  ohltquum 
the  ovum  becomes  much  elongated  before  the  first  division  occurs  (see  Bower  9, 
fig.  266). 


THE    EMBRYO 


47 


Till'  first  division  wall,  tlu'  basal  wall,  as  in  tin-  otlur  J.iispoiangiatjc,  is,  usually 
at  least,  transverse  to  the  axis  of  the  archcgoniuni  (Hg.  28,  A),  ilach  of"  the  cells  thus 
formed  is  next  divided  by  a  vertical  wall,  so  that  the  embryo  is  dividc<l  into  approxi- 
mately equal  quadrants.  Jeffrey  states  that  the  quadrants  are  next  divided  by  a 
third  (transverse)  wall,  so  that  there  is  a  regular  octant  formation  (Jeffrey  I,  page 
16),  but  adds  that  this  segmentation  presents  various  irregularities  and  this  is 
confirmed  by  my  own  studies  of  the  young  em- 
bryo. In  B.  lunaria,  according  to  Bruchmann, 
the  octant  divisions  are  very  regular. 

In  B.  vtrglniiitiiim  the  young  embryo  is 
often  somewhat  pointed  above,  and  transverse 
divisions  of  such  embryos  may  show  that  the 
octant  formation  is  suppressed  in  the  epibasal 
region,  and  this  tapering  upper  part  of  the  young 
embryo  suggests  a  suspensor  similar  to  that  de- 
veloped' tin  Daima,  but  less  clearly  defined,  and 
probably  not  determined  by  the  first  division  of 
the  embryo.  Whether  the  suspensor  found  by 
Lyon  in  B.  obliquinn  (Lyon  1)  originates  in  a 
similar  fashion  remains  to  be  seen.  This  elonga- 
tion of  the  upper  part  of  the  embryo,  whether  it 
is  considered  as  a  suspensor  or  not,  is  doubtless,  as  Jeffrey  has  suggested,  useful 
in  pushing  the  developing  embryo  deeper  down  into  the  prothallial  tissue. 

For  some  time,  only  anticlinal  walls  are  formed,  this  showing  especially  plainly 
in  transverse  section  (fig.  31).  Sooner  or  later  periclinal  walls  are  also  formed,  and 
it  is  possible  that  in  some  cases  the  first  periclinal  wall  in  one  of  the  large  epibasal 
cells  may  establish  the  initial  cell  of  the  root,  but  this  is  hard  to  decide.  The  early 
stages  of  the  embryo  are  extremely  difficult  to  embed  without  shrinkage,  and  this, 
together  with  the  difficulty  of  securing  a  sufficient  number  of  the  right  stages  and 
the  impossibility  of  regulating  the  direction  in  which  they  are  cut,  makes  the  deter- 
mination of  the  origin  of  the  primary  organs  of  the  young  embryo  a  peculiarly 
difficult  problem. 


,  30. — Three  longitudi 
embryo  of  Bolrychi 
root;  /,  the  foot.    ) 


Neither  |effrey  nor  Bruchmann  was  able  to  recogni/e  a  root  initial  until  the 
embryo  had  attained  a  large  size,  and  its  origin  could  not  be  determined.  In  the 
embryo  shown  in  fig.  :50,  I  am  inclined  to  believe  that  the  cell  r  is  really  the  root 
initial.  Unfortunately,  stages  between  this  and  the  one  shown  in  fig.  32,  where  the 
root  initial  is  unmistakable,  were  wanting,  but  the  position  and  state  of  develop- 
ment of  the  root  in  the  latter  harmonize  with  this  supposition.  My  fig.  32  is  evi- 
dently of  about  the  same  size  as  Jefl^rev's  fig.  46,  and  probably  an  examination  of 
other  sections  of  the  series  from  which  Jeffrey's  figure  was  drawn  would  show  the 
root  initial,  as  well  as  traces  of  the  stem  apex  and  cotyledon. 


48 


THE    OPHIOGLOSSALES 


All  of  the  organs  of  the  young  sporophyte  arise,  as  Jeffrey  showed,  from  the 
epibasal  region,  and  in  this  respect  Botrychium  virgtnianum  agrees  with  the  Marat- 
tiaceae  and  with  Ophioglossum.  According  to  Bruchmann,  the  embryo  in  B.  lunaria 
remains  quite  undifferentiated  up  to  the  time  it  breaks  through  the  calyptra,  even 
the  root  apex  being  unrecognizable  at  this  time.  It  is  therefore  impossible  to  say 
what  relation  the  organs  of  the  young  sporophyte  bear  to  the  primary  divisions  of 
the  embryo. 


b  h,  basal  wall;   /,  foot; 


In  B.  virginianum  traces  of  the  quadrant  formation  are  still  evident  at  a  com- 
paratively late  stage,  and  there  seems  no  reason  to  doubt  the  correctness  of  Jeffrey's 
conclusion  as  to  the  epibasal  origin  of  both  the  root  and  the  cotyledon.  As  in 
Ophioglossum  pendulum  and  O.  vulgatum,  the  root  is  especially  conspicuous  and 
reaches  a  large  size,  while  the  stem  apex  and  cotyledon  are  still  inconspicuous. 
Indeed,  in  B.  lunaria,  according  to  Bruchmann,  no  trace  of  either  stem  apex  or 

cotyledon  can  be  made  out 
until  the  root  has  broken 
through  the  calyptra.  At 
this  stage  (fig.  36,  C,  D) 
the  embryo  of  B.  lunaria 
bears  a  striking  resem- 
blance to  that  of  Ophio- 
glossum vulgatum. 

It  was  found  by  Jef- 
frey in  B.  virginianum 
that  the  stem  initial  was 
developed  before  the  co- 
tyledon could  be  seen,  but 
I  have  failed  to  verify  this 
in  the  specimens  I  have 
examined.  Fig.  32  shows 
three  sections  of  a  series 
taken  from  an  embryo  of 
about  the  age  of  Jeffrey's  fig.  46.  I'his  embryo  was  cut  transversely  to  its  long  axis, 
and  the  root  apex  is  thus  seen  in  cross-section.  1  he  root  here  probably  comprises 
the  whole  of  one  of  the  epibasal  quadrants,  from  the  other  of  which,  or  from  part  of 
it,  perhaps  a  single  octant,  the  stem  apex  and  cotyledon  arise  in  close  proximity.  It 
is  probable  that  part  of  this  quadrant  goes  to  form  the  "  suspensor,"  or  that  epibasal 
tissue  which  is  not  concerned  in  the  formation  of  the  young  organs  of  the  embryo. 
Fig.  32,  B  shows  a  section  passing  through  the  young  cotyledon,  whose  single  apical 
cell  is  already  differentiated.  This  in  section  is  triangular,  and  the  cell  is  probably 
of  tetrahedral  shape.     Fig.  32,  C,  shows  the  section  passing  through  the  stem  apex. 


49 


Piobahlv  the  large  cell  {st)  is  the  apical  cell,  hut  this  is  not  ahsolutely  certain.  In 
foini  and  position  this  cell  resembles  the  apical  cell  figured  by  JcttVey  (Jeffrey  I, 
fig.  48)  in  an  older  embryo.  It  may  be  said  that  in  Jeffrey's  figure  the  beginning  of 
the  cotyledon,  situated  between  the  stem  apex  and  the  root,  although  not  lettered,  is 
evidently  present. 

As 'the  embryo  grows  the  loot  rapidl)  increases  in  length,  and  together  with  the 
foot  comprises  the  greater  part  of  the  embryo.  The  foot  is  very  large,  usually 
nearly  hemispherical  in  foim,  but  not  infrequently  a  good  deal  elongated  (fig.  35), 
and  penetrates  deep  into  the  prothallial  tissue. 

The  apical  cell  of  the  root  is  very  conspicuous  and  can  be  made  out  without 
difficulty  as  a  large  cell,  triangular  in  form,  whether  it  is  viewed  in  longitudinal  01 
transverse  section.  Segments  are  cut  off  in  regular  sequence  from  all  of  the  four 
faces,  and  as  these  are  relatively  large  and  contain  but  little  granular  contents  the 
apical  meristem  sho\\s\ei\  cltarly  against  the  smaller  celled  and  more  deeply  stained 


A-C.  Three  horizontal 
D.  The  stem  region 


adjacent  tissue.  In  the  earlier  stages  the  divisions  in  the  segments  cut  oH  fmni  the 
apical  cell  do  not  show  absolute  uniformity.  The  first  wall  in  the  young  segment  is 
probabU-  anticlinal,  and  seems  to  be  followed  by  a  periclinal  wall  or  walls,  cutting 
off  inner  cells  which  contribute  to  the  very  large  plerome  cylinder  ot  the  young  root. 
The  root  cap,  which  is  very  massive,  is  derived  in  part  from  segments  cut  oft  directl\ 
fiom  the  apical  cell,  and  in  part  from  cells  separated  by  periclinal  walls  from  the 
outer  part  of  the  lateral  segments  of  the  apical  cell. 

The  development  of  the  plerome  begins  very  early,  and  it  soon  forms  a  con- 
spicuous massive  strand  of  procambium  cells  extending  from  tlu'  root  apex  to  the 
junction  of  the  root  antl  foot,  where  it  ends  abruptly  on  the  lower  side,  but  bends 
upward  on  the  upper  side,  and  is  extended  as  a  simjile  axial  strand  of  tissue  into  the 
cotyledon. 

The  cotyledon,  which  is  first  recognizable  at  an  early  stage  in  the  development 
of  the  embryo,  at  the  stage  in  question  (fig.  35,  J)  projects  slightly  as  a  broad,  flat- 
tened cone,  strongly  bent  away  from  the  root.    Fig.  34.  //,  shows  the  cotyledon  cut 


50 


THE    OPHIOGLOSSALES 


through  horizontally.  At  the  slightly  projecting  apex  there  is  a  single  apical  cell, 
although  it  is  not  always  quite  certain  which  is  the  apical  cell  and  which  is  its 
youngest  segment.  The  broad  base  of  the  cotyledon  is  extended  laterally,  like  the 
stipules  of  the  older  leaves,  and  there  is  thus  inclosed  a  slightly  depressed  area,  very 
much  as  in  the  embryo  of  Ophtoglossum  vidgatum,  and  within  this  is  situated  the 
stem  apex,  close  to  the  base  of  the  cotyledon,  which  bends  over  it  so  as  to  leave 
only  a  narrow  space  above  the  stem  apex.  A  section  across  the  base  of  the  cotyledon 
shows  a  group  of  small  cells  indicating  the  section  of  the  young  vascular  bundle 
which  lower  down  (fig.  34,  C)  joins  the  young  bundle  of  the  primary  root. 

The  relative  position  of  the  young  organs  just  before  the  root  ruptures  the 
calyptra  is  best  seen  in  a  longitudinal  section.  Such  a  section  (fig.  35,  A)  shows  the 
very  large  foot,  occupying  approximately  half  of  the  embryo,  and  deeply  embedded 
in  the  prothallium.  Above  this  is  the  root,  occupying  the  major  part  of  the  epibasal 
region  of  the  embryo  and  varying  somewhat  in  position,  perhaps  due  to  the  early 
divisions  in  the  young  embryo.  It  may  lie  in  a  plane  almost  coincident  with  the 
cotyledon,  or  it  may  make  a  marked  angle  with  the  latter.     In  the  former  case  the 


Fig.  35. 


Median  section  of  a  young  sporophyte  of  Botr 
An  older  stage;  /',  second  leaf;  r^,  second  i 


young  vascular  cylinder  is  continued  almost  straight  into  the  cotyledon;  in  the 
latter  it  bends  sharply  upward  to  meet  it. 

The  stem  apex,  which  is  usually  more  or  less  oblique,  is  small  and  incon- 
spicuous, but  usually  a  single  initial  cell  may  be  made  out  without  difficulty,  although 
sometimes  it  is  not  easy  to  distinguish  this  from  the  younger  segments  which  have 
been  cut  off  from  it,  as  the  apical  meristem  is  very  shallow,  and  in  longitudinal 
section  has  the  appearance  of  a  columnar  epithelium.  There  seems  to  be,  at  least 
in  the  earlier  stages  of  development,  some  variation  in  the  form  of  the  initial  cell, 
which  may  have  a  pointed  base,  or  may  be  truncate  below,  and  while  later  it 
usually  shows  the  form  of  a  three-sided  pyramid,  in  these  earlier  stages  it  often 
approximates  the  truncate  form  found  in  Ophioglossum  moluccanum. 

The  apical  meristem  of  the  stem  is  very  limited  in  extent  and,  so  far  as  could 
be  made  out,  the  segmentation  at  first  does  not  follow  any  regular  scheme.  While 
in  both  root  and  cotyledon  a  central  strand  of  procambium  is  developed  at  a  very 
early  period,  no  trace  of  anything  which  can  he  interpreted  as  a  "stele"  is  formed  in 
the  young  stem.  The  tissues  derived  from  the  further  segmentation  of  the  apical 
meristem  remain  undifferentiated  parenchyma  and  contribute  only  to  the  central 
pith   of  the  hollow  woody  cylinder  which    later   traverses  the  axis  of  the  young 


THI-:    EMBRYO  51 

sporophyte.  In  short,  the  strand  of  vascular  tissue  in  the  young  sporophyte  at  the 
time  the  first  root  emerges  is  composed  solely  of  the  cf)alescent  strands  of  the  root 
and  leaf  exactly  as  is  the  case  in  the  young  sporophyte  of  Ophioglossinn  nioluicinnitti, 
and  there  is  absolutely  no  trace  of  a  cauline  stele. 

The  foot  is  composed  of  large  parenchyma  cells,  which  become  smaller 
toward  the  periphery,  where  they  usualh'  sliowmoreor  less  dense  contents  and  some- 
times form  a  quite  definite  laycrof  epithelium-like  cells,  which  stain  much  more  deeply 
than  the  inner  tissue  of  the  foot.  This  outer  layer  of  cells  is  presumably  active  in 
the  absorption  of  nutriment  from  the  adjacent  prothallial  tissue.  Bruchmann  states 
that  previous  to  the  emergence  of  the  root  of  the  young  sporophyte  of  B.  liuuiria 
the  cells  of  the  embryo  are  densely  packed  with  granular  matter  of  apparently 
albuminous  nature;  but  after  the  emergence  of  the  root  starch  is  developed  abun- 
dantly in  the  cells  of  the  foot.     This  appears  to  be  true  also  of  i^.  virgtmanuni. 

Compared  with  B.  virgininniim,  the  embryo  of  5.  lunaria  (fig.  36)  is  character- 
ized by  the  lesser  development  of  the  foot  and  the  later  appearance  and  rudimentary 
character  of  the  stem  apex  and  the  cotyledon. 

The  stem  apex  in  B.  liuiana  (Bruchmann  2)  is  first  evident  as  a  slight  sujierfi- 
cial  depression  near  the  base  of  the  massive  root.  A  single  superficial  cell  becomes 
differentiated  as  the  apical  cell  of  the  shoot,  and  a  small  group  of  cells  is  formed 
before  the  rudimentary  cotyledon  develops.  Both  stem  apex  and  cotyledon  remain 
very  inconspicuous.  The  cotyledon  is  developed  as  a  scale-like  rudiment,  which 
never  develops  into  a  foliage  leaf.  Bruchmann  states  (Bruchmann  2,  page  223) 
that  from  seven  to  nine  of  these  rudimentary  leaves  are  developed  before  the  first 
green  leaf  appears  above  the  earth.  Hofmeister  (Hofmeister  1)  believed  that  three 
of  these  rudimentary  leaves  were  developed  during  the  first  year,  and  that  the 
second  year  the  first  spore-bearing  leaf  appeared  above  ground.  Bruchmann  thinks 
that  this  is  not  the  case  and  that  the  first  spore-bearing  leaf  requires  five  years  for  its 
development,  as  it  does  in  the  older  sporophytcs,  and  that  only  o\w  leaf  is  formed 
each  year,  as  in  the  older  plant. 

The  first  organ  to  penetrate  the  calyptra  is,  as  we  have  seen,  the  root,  which  in 
B.  virgin  I  aiitit?!  is  very  large  and  quite  overshadows  the  relatively  inconsjiicuous 
bud  at  its  base  (fig.  7,  B).  At  the  time  the  root  first  emerges  the  vascular  bundles 
still  have  the  form  of  procambium,  and  it  is  not  until  the  young  root  has  a  length  of 
several  millimeters  (5  to  20  millimeters,  according  to  Jeffrey)  that  the  first  tracheary 
tissue  is  developed.  The  first  tracheary  tissue  arises  at  the  base  of  the  root  and  the 
development,  as  usual,  proceeds  toward  the  apex.  The  primary  root  in  Botrvclinnn 
virginiauiim  is  usually  diarch,  but  triarch  roots  are  sometimes  found,  and  leffrey 
says  that  the  size  of  the  root  has  no  relation  to  the  number  of  proto.xylems  formed. 
The  first  tracheids  are  short  and  reticulately  marked,  as  they  are  in  Ophioglossum. 
The  surface  of  the  root  is  quite  destitute  of  root  hairs,  as  is  the  case  in  the  adult 
sporophyte. 

In  B.  limaria  the  puclominance  of  the  root  over  the  shoot  is  even  more  marked 
than  in  B.  vngiiuaiunu,  for  tin  re  are  se\eral  roots,  sometimes  four  to  fi\e,  ilevelopcd 
before  the  first  foliage  leaf  is  formed,  and  the  bud  remains  extremely  small  and 
inconspicuous. 

A  longitudinal  section  of  the  cot\ledon  of  i?.  virginiaiiiitru  just  before  it  breaks 
through  the  overlying  cahptra,  shows  it  to  be  strongly  curved  awa\-  from  the  root 
and  overhanging  the  cleft  within  which  lies  the  stem  apex.  If  the  section  is  exactly 
a  median  one,  there  may  be  seen  near  the  tip,  but  lying  somewhat  toward  the  lower 
side,  a  marginal  cell  of  triangular  outline,  which,  from  the  arrangement  of  the  cells 
about  it,  is  evidentU'  the  apical  cell.    The  cotyledon,  instead  of  being  straight  as  it 


52 


THE    OPHIOGLOSSALES 


is  in  Ophioglosstim  and  Botryiliiiim  huioria,  approaches  the  circinate  form  of  that  of 
the  Marattiaceae  and  the  typical  ferns.  The  young  vascular  bundle  is  now  clearly 
evident,  lying  somewhat  toward  the  inner  side  of  the  leaf,  and  it  can  be  readily 
followed  downward  until  it  joins  the  root  bundle,  with  which  it  is  continuous. 

In  B.  virginianutn,  while  the  cotyledon  is  still  quite  small,  the  second  leaf 
appears  close  to  the  stem  apex  and  nearly  opposite  the  cotyledon,  the  sheathing 
base  of  which  surrounds  the  stem  apex,  together  with  the  young  second  leaf.  The 
growth  of  the  second  leaf  is  also  probably  from  a  tetrahedral  apical  cell,  and  this 
is  the  case  with  all  of  the  later  leaves.  While  the  second  leaf  is  still  very  small, 
there  begins  the  differentiation  of  the  corresponding  leaf  trace,  which  joins  the 
bundle  of  the  primary  root  close  to  the  point  at  which  it  gives  off  another  bundle 
destined  for  the  second  root,  the  apical  cell  of  which  is  cut  out  from  the  tissue  near 
the  base  of  the  second  leaf,  at  a  point  almost  directly  opposite  the  cotyledon. 
Indeed,  the  second  root  may  be  said  to  bear  much  the  same  relation  to  the  second 
leaf  that  the  primary  root  does  to  the  cotyledon  (fig.  35,  B). 


Fin.  36. — Bolryclilum  lunaria  (after  Bruchmann). 


The  cotyledon  in  B.  virgtniaiium  (fig.  7)  is  extraordinarily  developed,  reaching 
a  size  that  probably  is  unequaled  by  any  other  fern.  Its  slender  petiole  reaches 
a  length  of  5  to  6  centimeters,  and  the  lamina,  unlike  the  simple  oval  primary  leaf  of 
Ophioglossiim,  is  ternately  divided  and  the  segments  deeply  cut.  The  venation, 
instead  of  being  reticulate  as  in  Ophioglossiim,  is  apparently  pinnate,  but  this  is 
really  the  result  of  an  unequal  dichotomy,  as  it  is  in  the  ultimate  branches  of  the 
veins  in  most  ferns. 

The  base  of  the  petiole  forms  a  stipular  sheath  like  that  found  in  the  later 
leaves,  and  it  is  traversed  by  two  vascular  bimdlcs,  which  unite  into  a  single  trace 
before  joining  the  bundle  of  the  root. 

While  in  B.  hinaria  all  of  the  early  leaves  remain  rudimentary,  and  the  first 
one  to  appear  above  ground  is  a  fertile  one,  there  are  sometimes  intermediate  stages 
which  may  show  a  small  ternate  lamina  and  traces  of  the  fertile  spike,  although  they 
never  appear  above  ground  (see  Bruchmann  2,  fig.  50). 

If  horizontal  sections  of  the  young  sporophyte  are  examined,  at  about  the  time 
the  cotyledon  first  emerges  (fig.  41),  the  latter  will  be  seen  to  have  the  form  of  a 


THE    rMr.KVO  53 

crescent,  the  horns  of  wliich  unite  at  ahout  the  le\el  of  the  stem  apex,  so  that  the 
latter,  together  with  the  section  of  the  seccjnd  leaf,  is  completely  inclosed  by  the 
sheath  formed  at  the  base  of  the  cotyledon.  The  leaf  trace  in  both  the  cotyledon 
and  the  second  leaf  is  broadly  oval  in  outline,  increasing  in  breadth  lower  down, 
so  that  the  section  there  becomes  crescent-shaped  and  the  two  together  form  an 
imperfectly  closed  ring  of  small  cells,  the  procambiiim  of  the  future  vascular  cyl- 
inder of  the  axis,  which  clearly  is  formed  entirely  from  the  united  leaf  traces. 

The  apical  cell  of  the  stem  appears  triangular  in  cross-section,  and  from  it  are 
cut  off  regular  segments,  but,  as  we  have  seen  from  the  study  of  the  longitudinal 
section,  the  tissues  which  are  developed  from  these  segments  below  the  apical  cell 
remain  undifferentiated  and  form  merely  a  mass  of  large  parenchyma  cells  with 
thin  walls,  which  fill  the  space  within  the  ring  formed  b\-  the  confluent  leaf  traces, 
and  thus  constitute  the  pith  or  medulla  of  the  stem. 

Jeffrey  (Jeffrey  1,  page  19)  refers  to  the  occurrence  of  short  tracheids  in  the 
prothallial  tissue  in  one  case  which  came  under  his  observation.  Theie  was  seme 
evidence  that  an  embryo  had  been  present,  but  it  had  disappeared,  and  he  thought 
it  possible  that  this  was  a  case  of  apogamy,  similar  to  that  which  has  been  repeatedly 
observed  in  Ptens  crettca  and  in  various  other  leptosporangiate  ferns.  If  apogamy 
does  really  exist  in  B.  virginuuuitti  it  is  the  only  case  which  is  known  amon<^  the 
Eusporangiatx> 

Botrychnnii  obliqiiiim  (Lyon  1)  differs  strikingly  in  the  foim  of  the  eml)r\() 
from  either  B.  virguiiainini  or  B.  Imuiria,  and  these  differences  are  so  marked  that 
Lyon  proposes  to  separate  B.  obliquum  and  a  number  of  allied  species  as  a  new 
genus,  Sceptridium.  The  ovum  in  Botrvcliium  obliquum  becomes  very  much 
elongated  after  fertilization,  and  it  is  probable  that  the  first  wall  separates  the  part 
next  the  archegonium  from  the  inner  cell,  the  former  developing  into  a  suspensor, 
very  much  as  we  shall  see  that  it  does  in  Dancea,  and  this  suspensor  becomes  well 
developed  and  is  conspicuous  in  the  later  stages  of  the  embryo.  Unfortunately, 
Lyon  gives  no  details  of  the  further  history  of  the  embryo  until  the  definitive  organs 
are  far  advanced.  He  states  that  the  suspensor  becomes  elongated,  pushing  down 
the  rest  of  the  embryo,  which  he  calls  the  "protocorm,"  believing  that  it  is  homol- 
ogous with  the  so-called  "protocorm"  of  Lvcopodiuni — a  resemblance  which  would 
probably  disappear  were  a  more  thorough  study  of  the  subsequent  history  available. 
This  development  of  a  suspensor  is  the  first  case  described  in  the  ferns,  but,  as  we 
shall  see  presently,  a  similar  suspensor  is  regularly  present  in  the  genus  Dancca, 
which  in  other  respects  shows  some  interesting  resemblances  to  B.  obliquum  in  the 
development  of  the  embryo.  Moreover,  as  we  have  seen,  there  is  often  an  elonga- 
tion of  the  upper  cells  of  the  \'oung  embryo  of  B.  virginianitm,  which  suggests  a 
rudimentary  suspensor. 

Lyon  figures  only  a  very  advanced  stage  of  the  embryo,  at  about  the  time  when 
the  root  first  emerges  from  the  prothallium.  At  this  time,  aside  from  the  presence 
of  the  suspensor,  the  most  marked  difference  between  B.  obliquum  and  B.  virgin- 
iaiium  is  the  apparent  absence  of  the  foot  in  the  former  species,  while  this  organ  is 
so  remarkably  developed  in  B.virginianum.  The  root  \nB.  obliquum  penetrates  the 
lower  surface  of  the  gametophyte,  the  cotyledon  breaking  through  on  the  upper 
side,  so  that  the  relative  position  of  the  leaf  and  root  is  like  that  of  Ophioglossum 
moluccauum,  or  the  Marattiace;e.  In  the  orientation  of  the  root  and  shoot,  there- 
fore, B.  obliquum  is  much  more  like  Dinuni  or  Opliioglossiim  molucciiiium  than  it 
is   like   B.  vitgiuianum. 

It  is  to  be  hoped  that  further  investigations  will  lu-  math-  u|ion  this  extrenieh 
interesting  species.     We  anticipate  that  when   the   histor\    of  the  earlier  stages  is 


54  THE    OPHIOGLOSSALES 

known  it  will  be  found  that  a  large  foot  is  present  in  the  embryo,  as  it  is  in  the 
Marattiaceae  and  the  other  Ophioglossaceae,  and  the  apparent  absence  of  this  foot 
in  the  older  embryo  is  due  to  the  root  apex  being  formed  deep  in  the  central  tissue 
of  the  embryo,  as  it  is  in  the  Marattiaceae  and  in  Ophioglossuni  moluccanum,  and 
pushing  its  way  downward  through  the  foot,  which  thus  becomes  indistinguishable 
from  the  outer  tissue  of  the  root. 

Except  for  the  absence  of  the  foot  the  organs  of  the  older  embryo  of  5.  oblt(juum 
show  the  same  relative  positions  as  those  of  B.  virginiatnim,  and,  as  in  the  latter, 
the  first  leaf  is  apparently  a  functional  green  leaf  which  appears  above  the  surface 
of  the  earth. 

THE  EMBRYO  OF  HELMINTHOSTACH^'S. 

The  embryogeny  of  Helmtnthostachys,  the  third  genus  of  the  Ophioglossaceae, 
is  unfortunately  very  incompletely  known.  Lang  (Lang  I),  to  whom  we  owe  the 
only  published  account  of  the  gametophyte  and  young  sporophyte,  was  unable  to 
secure  any  young  embrj^os  and  only  very  scanty  material  of  the  later  stages.  Lang 
says  of  the  youngest  forms  which  he  found  (Lang  1,  page  40): 

"The  large  hemispherical  foot  is  deeply  inserted  in  the  tissue  of  the  prothallium. 
The  upper  portion  of  the  embryo  had  burst  through  the  covering  also  of  the  latter; 
in  it  can  be  distinguished  the  primary  root — the  first  leaf— and  (covered  over  by 
the  sheath  of  the  first  leaf)  the  depressed  apex  of  the  stem.  The  position  of  the 
organs  is  thus  essentially  similar  to  what  is  found  in  Botrychiiim  virgintanmn." 

Lang's  material  was  collected  in  the  Barrawa  Reserve  Forest,  in  Ceylon,  and 
in  February  1906  I  visited  the  same  locality  and  collected  a  large  number  of  young 
sporophytes,  many  of  which  were  still  connected  with  the  gametophyte;  but  none 
of  the  gametophytes  were  young  enough  to  show  young  embryos.  As  we  have 
already  suggested,  it  seems  very  probable  that  the  gametophyte  of  HehnintJi- 
ostachys,  like  that  o{ Ophioglossum  nioluccaiuim,  is  annual  and  produces  normally  a 
single  sporophyte,  after  which  it  perishes.  The  development  of  the  gametophyte  is 
probably  dependent  upon  the  annual  inundation  of  the  forest,  and  this  perhaps 
accounts  for  the  fact  that  all  of  the  young  sporophytes  were  of  about  the  same  age. 

The  youngest  specimen  which  I  found  is  shown  in  fig.  10.  The  petiole  of  the 
leaf  was  about  i  centimeter  in  length,  and  at  the  tip  the  minute  lamina,  strongly 
bent  over  like  the  young  leaves  oi  Botrychiiim  vtrgtnianurn,  could  be  seen,  showing 
the  three  lobes  which  characterize  the  fully  expanded  leaf.  The  cotyledon  is  rudi- 
mentary in  Hehninthostachys,  the  "cotyledon"  described  by  Lang  being  really  the 
second  leaf.  At  the  base,  but  separated  from  the  root  by  a  short  internode,  is 
a  swelling  which  marks  the  position  of  the  apical  bud,  inclosed  within  the  hollow 
sheath  at  the  base  of  the  petiole.  The  root  at  this  stage  is  still  quite  short,  the  first 
green  leaf  seeming  to  be  more  precocious  than  in  Botrychium  and  thus  resembling 
Ophioglossuni  moluccanum. 

As  the  leaf  grows  the  lamina  expands  and  is  seen  to  be  ternate  in  form.  Very 
often  the  two  lateral  lobes  are  of  unequal  size  and  show  that  the  ternate  form  is  due 
to  an  unequal  dichotomy,  such  as  is  common  in  many  ferns  in  the  early  leaves,  which 
are  transitional  between  the  dichotomously  divided  cotyledon  and  the  pinnate 
leaves  of  the  older  sporophyte.  The  ultimate  divisions  of  the  veins,  as  in  Botrych- 
ium, are  dichotomous.* 

*  In  a  recent  note  (Lang  2)  it  is  stated  that  a  suspensor  also  occurs  in  Helminthoitachys. 


55 


1.  rill'.  ^ouNc;  si'oRoi'iivi  1 


TilK  YOUNC;  Sl'OROl'll^'lK  OK  Ol'i  IIO(;LOSSUM. 

As  we  have  seen,  the  single  vascular  strand  in  the  young  sporophyte  of  Ophio- 
glossiim  rnoluccanum  is  continu<JUs  through  the  cotyledon  and  root,  and  sections 
at  different  heights  show  essentially  the  same  structure  throughout.  The  petiole 
of  the  cotyledon  (figure  27,  A),  which  is  traversed  by  two  conspicuous  lacunae, 
shows  that  the  axial  bundle  has  a  perfect  collateral  structure.  The  xylem  consists 
of  a  group  of  about  a  half  dozen  tracheids  on  the  inner  side  of  the  bundle,  of  which 
the  endodermis,  however,  is  not  evident.  If  a  section  made  in  the  mid-region  of 
the  plant  is  examined,  the  only  difference  between  its  bundle  and  that  within  the 
petiole  of  the  leaf  consists  in  the  somewhat  greater  development  of  the  tracheary 
tissue.  The  section  of  the  root  bundle  also  almost  exactly  resembles  that  of  the  leaf". 
Whether  we  call  tln'  root  bundle  monarch  or  collateral  is  merely  a  question  of  terms. 


ng  sporophyte  of  Ofiliio^hnum 
developed;  r,  primary  root  of  sporophyte;  r',  first  root  of  bud; 
D.  The  stem-apex  more  liighly  magnified,  showing  the  third  leaf,  /^. 

In  the  mid-region  of  the  sporophyte  the  endodermis  is  well  marked,  and  this  is  even 
more  the  case  in  the  root.  In  the  mid  region  the  xylem  is  separated  from  the  endo- 
dermis by  a  single  layer  of  pericycle  cells. 

About  the  time  that  the  leaf  emerges  the  first  root  of  the  bud  begins  to  develop, 
and,  like  the  leaf,  it  seems  to  arise  quite  independently  of  the  stem  apex.  The 
tetrahedral  apical  cell  is  cut  out  from  the  cortical  tissue  of  the  root  some  distance 
below  the  apex  of  the  young  bud,  and  as  soon  as  the  apical  cell  is  established  active 
segmentation  begins  in  the  tissue  below  the  bud  and  a  strand  of  procambium  is 
developed,  connecting  the  young  root  apex  directly  with  the  vascular  bundle  of  the 
primary  root.  Thus  the  vascular  bundles  of  both  the  first  leaf  and  the  first  root  of 
the  young  bud  are  directly  connected  with  the  primary  root  of  the  young  sporo- 


phyte and  have  nothing  to  di 
which  is  still  very  small. 


ith  rhi 


the 


ipex 


)t  the  stem  ot  tlu'  Inu 


56  THE    OPHIOGLOSSALES 

The  two  bundles,  belonging  respectively  to  the  leaf  and  the  root  of  the  bud, 
join  the  bundle  of  the  primary  root  very  near  together,  and  from  near  this  point  of 
junction  the  development  of  the  tracheary  tissue  proceeds  toward  the  apices  of  the 
young  organs.  The  first  tracheids,  like  those  found  m  the  median  region  of  the 
young  sporophyte,  are  short  reticulate  ones. 

The  first  leaf  of  the  bud  grows  rapidly  and  closely  resembles  the  cotyledon  in 
form  and  size,  and  at  first  it  often  looks  as  if  two  young  sporophytes  of  equal  size 
were  growing  from  the  prothallium,  but  a  very  slight  examination  shows  that  the 
second  leaf  belongs  to  the  bud  upon  the  primary  root.  The  second  leaf  of  the  bud 
also  seems  to  be  formed  independently  of  the  stem  apex  and  arises  nearly  opposite 
the  first  one  (fig.  37,  A).  Its  development  is  practically  the  same  as  that  of  the 
first  leaf,  and  it  pushes  through  the  outer  tissue  of  the  root  at  a  point  removed  by  an 
appreciable  distance  from  the  base  of  the  first  leaf,  from  which  it  is  separated  by  a 
sheath  about  the  base  of  the  latter,  formed  by  the  outer  root  tissues. 

The  vascular  bundle  in  the  second  leaf  is  soon  developed  and  can  be  followed 
down  to  the  bundle  of  the  first  root  of  the  bud,  to  which  it  bears  somewhat  the  same 
relation  that  the  bundle  of  the  first  leaf  of  the  bud  does  to  the  primary  root  of  the 
sporophyte.  Fig.  37  will  show  clearly  the  arrangement  of  the  vascular  bundles  in 
a  young  bud  in  which  the  first  leaf  is  fully  developed,  while  the  second  and  third  are 
pretty  well  advanced.  The  latter  (/^)  shows  very  plainly  the  conspicuous  apical 
cell  and  the  beginning  of  the  leaf  trace.  The  apical  cell  of  the  stem  at  this  time  is 
sufficiently  conspicuous,  but  the  amount  of  tissue  surrounding  it  is  quite  limited 
in  extent.  In  fig.  37,  D,  it  is  probable  that  the  fourth  leaf  has  begun  to  develop. 
Above  the  apex  of  the  stem  the  cavity  of  the  leaf  sheath  can  be  clearly  seen.  By 
this  time  the  first  root  of  the  bud  has  emerged  below  the  first  leaf  and  the  tracheary 
tissue  is  well  developed  in  its  basal  region. 

The  second  root  of  the  bud  originates  below  the  apex  of  the  stem  in  the  vicinity 
of  the  base  of  the  second  leaf.  The  vascular  strand  of  the  third  leaf  joins  it,  and  the 
third  leaf  seems  to  have  somewhat  the  same  relation  to  the  second  root  that  the 
second  leaf  does  to  the  primary  root. 

The  study  of  the  development  of  the  young  bud  shows  that,  up  to  the  time  of  the 
production  of  the  third  leaf,  the  young  organs  arise  quite  independently  of  each 
other  from  the  tissue  of  the  primary  root.  The  young  sporophyte  is,  so  to  speak, 
made  up  by  the  union  of  several  independent  members.  The  third  and  fourth 
leaves  arise  from  the  stem  apex  as  all  of  the  later  ones  do,  but  the  first  and  second 
leaves  and  the  first  root  show  no  recognizable  relation  to  the  stem  apex.  Their 
vascular  bundles  are  directly  connected  with  the  bundle  of  the  primary  root  of  the 
young  sporophyte,  and  are  in  no  way  associated  with  the  tissues  which  belong  to 
the  stem  region  of  the  bud.  No  material  was  available  for  the  study  of  the  origin 
of  the  leafy  bud  in  0.  pendulum,  but  the  first  leaf  evidently  develops  very  much 
later  than  it  does  in  O.  moliiccanum.  Young  leaves  10  centimeters  or  more  in  length 
were  found,  which,  there  is  some  reason  to  suppose,  were  the  primary  leaves  of  the 
young  plant;  but  they  were  not  recognized  as  such  at  the  time  they  were  collected 
and  it  is  therefore  impossible  to  say  whether  they  really  were  the  first  leaves  devel- 
oped. After  the  study  had  been  made  of  the  young  sporophyte  in  O.  mohiccanum, 
and  the  secondary  origin  of  the  stem  apex  was  made  out,  it  was  recognized  that  these 
small  leaves  in  (J.  pnuhilntu  also  were  probably  the  primary  leaves  of  the  plant,  but 
it  was  too  late  then  to  trace  the  connection  of  the  roots  from  which  they  developed 
to  their  connection  with  the  primary  root  of  the  young  sporophyte. 

I  was  unable  to  determine  just  how  soon  the  fertile  leaves  are  developed  from 
the  young  sporophyte  in  O.  moluccamnii.     In  all  of  the  specimens  that  were  sectioned, 


THK    YOIINC    SPOROIMIVTI 


57 


the  Hist  three  or  four  leaves  were  sterile  and  ]iraetHaliv  like  the  C()t\le(l()n,  and  it 
is  not  certain  which  leaf,  luulei  oidinaiv  circumstances,  first  gives  rise  to  the  spore- 
bearing  spike.  In  0.  moliiccanum  and  the  other  tropical  species  of  0/)hioglossum 
growth  is  continuous,  and  it  is  evident  that  the  development  of  the  leaves  does  not 
take  the  long  period  required  in  O.  vulgatum  and  other  species  of  temperate  regions, 
where  growth  is  interrupted  each  year  and  where  only  one  leaf  is  developed  in  the 


12:L\'^  z...-{J ''A^\ 


Sii  of  a  series  of  transverse  seclions  of  a  young  sporophyte  of  Ophioglossuin  moliiccanum,  still  attached  to  priirarj 
root,r.    Section  B  passes  through  the  stem  apei.     X35. 

season.  Mettenius  states  that  O.  pedunculosum,  which,  as  we  have  seen,  may  per- 
haps be  identical  with  0.  moluccanum,  develops  three  leaves  each  season.  1  his 
was  in  the  Botanical  Garden  at  Leipzig,  and  it  is  highly  probable,  under  the 
much  more  favorable  conditions  of  its  native  tropical  habitat,  that  this  number 
would  be  exceeded.  There  was  not  time  to  make  investigations  in  regard  to  this 
^  point,  but  it  is  very  certain 

that  several  leaves  are  de- 
veloped in  the  course  of  each 
year  and  that  the  develop- 
ment of  the  individual  leaf 
does  not  require  the  long  pe- 
riod necessary  in  the  species 
of  cold  climates. 

Figures  38  and  39  show 
several  transverse  sections 
forming  a  series  taken  from 
a  young  sporophyte  with 
three  fully  developed  leaves 
and  two  younger  ones.  This 
bud  was  developed  from  a 
small  root,  but  it  was  not 
certain  that  this  was  the 
primary  root  of  the  embryo. 
The  spirall)'  arranged  leaves 
show  the  two-fifths  diver- 
gence. The  seconti  ami 
third  leaves  of  this  Inul 
were  succes.sively  larger  than  the  first  leaf,  but  the  section  of  the  petiole  showed 
a  single  centrally  placed  vascular  bundle  of  the  same  type  as  that  ol  the  piimarv 


:ion  of  the  sporophyte  shown  in 
s  the  primary  root.     X  about  60. 
cular  bundle  of  first  leaf,  more  higlily  111 
n  apex,  showing  youngest  leaf  trace.  /*; 


3S,  she 


apical  cell  of  ; 


58  THE    OPHIOGLOSSALES 

leaf  and  all  of  these  leaves  were  sterile,  nor  could  any  indication  of  the  develop- 
ment of  a  central  spike  be  seen  in  the  development  of  the  fourth  leaf.  The  first 
leaf  of  the  bud,  like  the  cotyledon,  showed  two  large  lacunae  in  the  petiole,  but  in 
the  second  leaf  there  was  but  a  single  one  and  this  was  interrupted  at  intervals, 
while  the  petiole  of  the  third  leaf  appeared  almost  solid,  there  being  only  small, 
irregular,  intercellular  spaces,  such  as  are  always  found  in  any  loose  parenchyma. 
All  of  the  vascular  bundles  are  collateral.  In  the  lower  portion  of  the  third  leaf 
eleven  tracheids  could  be  seen  in  the  transverse  section  of  the  bundle,  but  higher 
up  the  amount  of  tracheary  tissue  was  reduced. 

Figs.  38,  A,  and  39,  A,  were  cut  just  above  the  stem  apex  and  showed  clearly 
the  arrangement  of  the  first  four  leaves.  The  youngest  leaf  is  still  entirely  surrounded 
by  the  conical  stipular  sheath  belonging  to  the  third  leaf.  Fig.  38,/^,  is  taken  imme- 
diately above  the  stem  apex  and  passes  through  the  very  young  fifth  leaf.  This 
section  shows  very  satisfactorily  the  arrangement  of  the  first  five  leaves.  Section  C 
lies  a  short  distance  below  the  stem  apex,  r  is  the  root  from  which  the  bud  has 
arisen,  and  the  group  of  tracheids  at  its  junction  with  the  bud  marks  the  point 
of  union  of  the  bundles  of  the  first  leaf  and  the  first  root  of  the  bud.  In  the  center 
of  the  section  may  be  seen  a  mass  of  large-celled  parenchyma,  the  central  pith  of  the 
stem,  which  is  derived  from  the  large-celled  meristem  of  the  stem  apex.  The  broken 
ring  of  procambium  surrounding  the  pith  is  composed  of  obliquely  cut  traces  of  the 
fourth  and  fifth  leaves  and  the  basal  tissue  of  the  second  root  of  the  bud.  The  leaf 
traces  from  the  second  and  third  leaves  are  still  free  in  the  cortical  tissue  of  the  young 
stem.  E  and  F  pass  through  the  base  of  the  bud.  The  stout  bundle  of  the  first 
root  is  seen  connected  with  the  bundle  of  the  root  upon  which  the  bud  was  developed, 
and  the  second  leaf  trace  (/'^)  bends  in  to  meet  the  bundle  of  the  root  but  is  cut 
at  a  level  above  the  point  of  junction.  Close  to  the  second  leaf  trace  is  the  lower 
part  of  the  fourth  leaf  trace,  which  is  connected  with  the  trace  of  the  second  root 
of  the  bud.  The  steles  of  both  the  first  and  second  roots  of  the  bud  run  horizon- 
tally across  its  base  before  they  emerge,  and  the  leaf  traces  are  almost  perpendic- 
ular to  these.  The  second  leaf  trace  at  the  base  of  the  bud  joins  the  stele  of  the 
first  root  and  the  short  tracheids  curve  out  trom  the  opposite  side  of  the  bundle  of 
the  first  root  to  unite  with  the  base  of  the  third  leaf  trace,  which  does  not,  as  might 
have  been  expected,  show  any  very  obvious  relation  to  the  second  root.  At  the 
point  where  the  first  root  bends  downward  to  emerge  from  the  overlying  cortical 
tissue  the  tracheary  tissue  of  this,  with  the  bases  of  the  leat  traces,  forms  a  large 
mass  of  irregular,  broad,  reticulate  tracheids,  occupying  the  center  of  the  base  of 
the  young  bud.  It  was  probably  the  presence  of  this  mass  or  tracheary  tissue  at  the 
base  of  the  bud  which  led  Rostowzew  to  state  that  the  bundle  of  the  bud  is  at  first 
solid.  It  is  possible  that  the  buds  formed  on  the  old  roots  ot  0.  vulgatum  may  be 
somewhat  different  in  structure  from  the  early  buds  in  O.  inoluccanum  and  that 
there  really  may  be  such  a  solid  stele  at  its  base. 

According  to  Rostowzew  (Rostowzew  1,  2)  and  Poirault  (Poirault  2),  the  buds 
upon  the  older  roots  ot  O.  vulgatum  usually  arise  close  to  the  apex,  much  as  they 
sometimes  do  in  the  formation  of  the  bud  upon  the  primary  root  of  O.  moluccanum. 
Van  Tieghem  thought  that  the  apex  of  the  root  itself  became  changed  into  the 
leafy  shoot,  but  both  Poirault  and  Rostowzew  demonstrated  that  the  young  bud 
originated  from  a  segment  of  the  apical  cell  of  the  root  and  not  from  the  apical 
cell  itself;  the  latter  continues  its  growth  and  the  root  thus  grows  beyond  the 
point  of  insertion  of  the  young  bud.  Rostowzew  states  that  an  outer  cell  of  the 
segment  divides  into  two  superimposed  layers,  of  which  the  superior  one,  or  the 
one  nearest  the  root  apex,  gives  rise  to  the  stem  apex  of  the  bud,  while  from  the  lower 


YOUNG    SPOROI'HVTr: 


59 


one,  i.  e.,  the  one  turned  toward  the  base  ot  the  root,  tlie  first  leaf  arises.  It  thus 
appears  that  in  these  adventitious  buds  in  Ophioglossum  viilgatiitn  there  is  much 
the  same  arrangement  of  the  first  organs  of  the  young  bud  that  we  have  seen  to  be 
the  case  in  O.  moluccanum,  the  leaf  and  the  stem  apex  being  virtually  independent 
organs.  From  Rostowzew's  figures  it  is  evident  that  the  bundle  from  the  first  leaf 
of  the  bud  in  O.  vulgatum  is  connected  directly  with  the  main  root  in  very  much 
the  same  way  as  it  is  in  the  primary  bud  in  ().  moliiccaiium;  but  apparently  the  first 
root  of  the  young  bud  is  inserted  higher  up  and  does  not  connect  directly  with  the 
primary  root;  this  point,  however,  needs  further  elucidation.  Moreover,  according 
to  his  statements,  there  is  a  good  deal  of  difference  shown  as  to  the  time  of  the  emer- 
gence of  the  leaves  and  roots,  three  or  four  roots  sometimes  being  well  developed 
before  the  first  leaf  expands.  This  reminds  one  of  the  behavior  of  tlie  primary 
sporophyte,  where  Bruchmann  found  that  sc\iral  roots  wvvv  developed  before  the 
first  green  leaf  made  its  appearance. 


40. — Vertical  secti 
right  angles  to  the 


young  sporophyte  of  Botrychium  virginumum.    llie  sections  were  c 
the  root.     sA,  stipular  sheath  of  cotyledon;    E,  section  of  primary 
in  this  case  was  triarch.     X20. 


THK  YOUNG  SPOROPHYTE  OF  BOTRYCHIUM. 

Jeffrey  (Jeffrey  1)  has  described  at  some  length  the  structure  of  the  young 
sporophyte  of  B.  virginiamnn,  and  Bruchmann  (Bruchmann  2)  has  studied  the 
earlier  stages  of  the  sporophyte  in  B.  lunarta.  The  present  account  is  based  mainly 
upon  my  own  studies  of  5.  vtrgiiiianum,  made  from  material  furnished  me  through 
the  kindness  of  Professor  Jeffrey.  Jeffrey  found  that  from  the  beginning  the  con- 
spicuous stele  found  in  the  axis  of  the  young  sporophyte  was  a  hollow  cylinder, 
which  he  assumes  to  be  a  really  cauline  structure,  and  not  made  up  of  leaf  traces. 
The  results  of  my  own  studies  indicate  that,  as  in  the  case  of  Opiitoglossuni,  the 
vascular  system  of  the  stem  is  made  up  exclusively  of  confluent  leaf  traces. 

Fig.  35,  /i,  shows  a  longitudinal  section  of  a  young  sporophyte  in  which  the  first 
two  leaves  are  evident  and  the  continuation  into  these  of  the  tissues  of  the  vascular 
bundle  of  the  root  is  very  clear.  The  large  central  pith  continues  up  into  the  stem 
apex,  but  the  whole  of  the  fibrovascular  tissue  is  continued  into  the  leaves,  there 


60 


THE    OPHIOGLOSSALES 


being  no  trace  of  procanibium  inside  of  the  leaf  traces  in  the  apical  region  of  the 
stem  itself.  Fig.  40  shows  a  sporophyte  which  was  cut  at  right  angles  to  the  primary 
root,  which  in  this  case  had  a  triarch  bundle.  Near  its  base  the  three  xylem  masses 
increase  in  size  and  form  a  nearly  complete  ring  of  tracheary  tissue,  which  higher 
up  is  continued  into  the  leaf  traces.  The  third  leaf  has  already  begun  to  form,  but 
is  still  very  small.  Below  it,  however,  can  be  clearly  seen  the  beginning  of  its  large 
leaf  trace,  which  can  be  followed  downward  to  its  junction  with  the  second  root, 
which  is  now  just  about  ready  to  emerge.  The  stele  of  the  second  root  is  con- 
nected with  the  central  cylinder  of  the  axis  near  its  junction  with  this  third  leaf 
trace.  1  he  stem  apex  occupies  a  very  small  area,  crowded  between  the  base  of  the 
second  and  third  leaves.  Its  deep,  narrow,  apical  cell  is  not  as  conspicuous  as  is 
often  the  case. 


s  through 


tern  apex, 


(,  which  1 


IS  of  a  young  sporophyte  of  Botrschium  virginianum.     X75. 
i  shown  more  enlarged  in  G;  r~,  second  root;  /^,  second  leaf. 


A  similar  sporophyte  is  shown  in  cross-section  in  fig.  41.  This  was  cut  in 
the  plane  of  the  first  root,  which  makes  a  sharp  angle  with  the  base  of  the  cotyledon. 
The  thick  stele  of  the  root  is  much  expanded  where  it  joins  the  leaf  traces  to  form 
the  beginning  of  the  tubular  stele  of  the  axis,  and  at  the  point  of  junction  there  is 
a  large  nearly  solid  mass  of  short,  irregularly  disposed,  reticulate  tracheids.  This 
young  sporophyte  was  evidently  the  further  development  of  an  embryo  of  the 
type  shown  in  fig.  35,  A.  The  trace  of  the  cotyledon  makes  a  right  angle  with  the 
stele  of  the  root  and  on  the  side  opposite  to  its  junction  with  the  stele  of  the  root 
there  can  be  seen  the  trace  belonging  to  the  second  leaf,  which  is  already  well 
developed.  The  apical  cell  is  tetrahedral  in  BrArychiurn  virginianum  and  the 
cells  are  cut  off  in  regular  .segments  from  its  three  lateral  faces.     Segmentation  is 


THK    YOUNG    Sl'OROPHYTE 


61 


evidently  slow  ami  there  is  usually  a  good  deal  of  difference  in  the  stage  of dexelop- 
ment  in  the  three  segments  composing  a  single  cycle.  The  first  division  in  each 
of  the  lateral  segments  cuts  off  a  small  inner  cell  from  a  large  outer  one,  and  the 
latter  is  then  divided  into  two  by  an  anticlinal  wall.  The  divisions  were  not  followed 
beyond  this  stage  and  the  limits  of  the  segments  comprising  the  .second  cycle  can 
not  be  easily  recognized,  as  by  this  time  the  youngest  leaf  begins  to  grow  and  the 
stem  apex  is  thus  crowded  into  a  ver\-  small  area  between  the  bases  of  the  two 
youngest  leaves.  The  shallow  mass  of  meristematic  tissue  comprising  the  stem  apex 
merges  gradually  into  the  large-celled  parenchyma  which  makes  up  the  pith  cylinder 
inside  the  hollow  stele  of  the  axis. 

Longitudinal  .sections  of  a  much  older  sporophyte  are  shown  in  fig.  42. 

Except  for  the  vascular  bundles,  the  whole  of  the  tissue  of  the  young  sporophyte 
is  composed  of  large-celled  parenchyma  which,  especially  in  the  region  belonging 
to  the  foot,  contains  large  quantities  of  starch. 

The  form  of  the  young  leaves  in  B.  virgiiiitnuuu  is  very  different  from  that 
in  B.  Innana.  In  the  former  the  young  leaf  is  bent  forward  over  the  stem  apex  and 
the  apical  cell  is  at  the  tip  of  this  bent-over  portion.     In  B.  Iiuitin'ti,  however,  the 


Three  longitudinal  sections  of  a  young  spor  )pliyte  of  Botrychtitm  virt^ittiatiutti  witli  sever 
/icr,  absciss  layer  of  peridirm,  /, /,  the  \oungest  leaves,  sh,  stipular  shcitli.      X20. 


\u 


bent-over  jiortion  becomes  the  stiimlai  legioii  and  the  apical  cell  of  the 
arises  in  the  convex  upper  portion,  so  that  the  leaf  grows  straight  u|iward  instead 
of  being  bent  over  as  it  is  in  B.  virgiiiKuuttii.  T!ie  latter  species  in  this  respect 
resembles   the   Marattiace:e. 

The  stipules  in  B.  vtrgniianiim  are  lateral  structures  which  exteml  around  the 
next  youngest  leaf  and  the  stem  apex,  but  the  sheath  has  a  nariow  cleft  in  front,  so 
that  we  may  really  speak  of  two  stipules  instead  of  a  single  stipular  sheath  (fig. 
42,  A^.     In  this  respect  also  there  is  a  strong  resemblance  to  the  Marattiaceap. 

Fig.  43  shows  a  series  of  transverse  sections  of  a  young  sporophyte  of  B.  vir- 
gintfiniitn  in  which  tlie  fourth  leaf  was  just  evident.  Fig.  4;5,  A  and  B,  are  near 
the  base  of  the  fourth  leaf  and  show  the  arrangement  of  the  first  four  leaves.  The 
base  of  the  cotyledon  {rot)  is  a  good  deal  flattened  and  the  petiole  is  seen  to  be 
traversed  by  very  conspicuous  lacunae,  reminding  one  of  those  in  the  cotyledon  of 
Ophioglossiim  mohiccanum.  The  conspicuous  stipules  can  be  seen  extending 
partly  around  the  group  of  younger  leaves,  but  not  completeh'  inclosing  them.  The 
two  vascular  bundles  of  the  petiole  are  beginning  to  unite  to  form  the  single  leaf 
trace  which  is  found  lower  down.    The  xylem  in  each  bundle  forms  a  broad  band 


62 


THE    OPHIOGLOSSALES 


of  wood,  which  is  surrounded  by  the  phloem,  although  the  latter  is  much  less 
developed  upon  the  inner  side  than  upon  the  outer  and  the  bundles  thus  approach 
the  collateral  condition  found  in  the  trace  lower  down.  Small  protophloem  ele- 
ments occur  in  the  outer  part  of  the  bundle  and  are  continued  part  way  around 
toward  the  lower  side,  to  the  point  where  the  two  bundles  are  beginning  to  fuse, 
but  here  they  are  no  longer  visible. 

The  second  leaf  shows  no  lacuna;  and  the  base  of  the  petiole  is  more  nearly 
cylindrical  than  is  that  of  the  cotyledon.  Like  the  latter,  the  petiole  contains  two 
vascular  bundles  which  at  the  level  of  this  section  were  still  quite  distinct,  and  the 
permanent  elements  were  just  beginning  to  form.  The  stipules  in  the  second  leaf 
completely  inclose  the  third,  but  there  is  a  very  narrow  slit  in  front  where  the  two 
stipules  meet.  The  next  section  figured  is  taken  just  above  the  stem  apex  and  cuts 
through  the  youngest  (fourth)  leaf.  The  two  bundles  of  the  petiole  of  the  third  leaf 
are  evidently  still  quite  separate,  but  closely  approximated,  and  as  yet  show  no  per- 
manent tissue.  The  stipules  of  the  third  leaf  are  just  becoming  evident.  At  the 
level  of  the  stem  apex  the  bases  of  the  third  and  fourth  leaves  are  completely  united, 


Scries  of  transverse  sections  of  a  young  sporophyte  of  Botryrlii 
cylinder.  D  and  E  show  the  separated  leaf  traces  whic 
its  junction  with  the  stele  of  the  primary  root. 


K  shows  the  bundle  of 


and  the  base  of  the  second  leaf  is  also  partially  fused  with  these.  The  two  bundles 
h'om  the  second  leaf  are  now  beginning  to  unite  to  form  the  single  leaf  trace,  while 
in  the  third  leaf  the  process  is  complete  and  a  single  oval  mass  of  procambium  cells 
marks  the  position  of  the  single  trace  of  this  leaf.  On  the  opposite  side  of  the 
apical  meristem  is  a  similar  but  less  developed  mass  of  procambium,  representing 
the  trace  from  the  young  fourth  leaf. 

For  some  distance  below  the  stem  apex  the  two  bundles  of  the  third  and  fourth 
leaf  respectively  are  quite  distinct,  and  are  separated  from  each  other  by  a  mass  of 
large-celled  pith.  Lower  down  the  two  bundles  approach  and  coalesce,  and  on  the 
side  of  the  second  leaf  trace  (which  is  turned  away  from  the  third  one)  a  group  of 
actively  dividing  cells  can  be  seen  which  forms  the  beginning  of  the  fifth  leaf  trace, 
although  the  leaf  itself  can  not  be  recognized  at  the  summit.  These  three  masses 
of  procambial  tissue,  viz,  the  young  traces  from  the  third,  fourth,  and  fifth  leaves, 


THK    VOUNG    SPOROl'HVTI 


63 


uiakea  iieaily  contiiiiiuuscrtscfnt-shapLd  massot  |ii()camhiuin.  Fig.  44,  .-V,/i,  shows 
the  section  of  the  central  stele;  and  the  space  between  the  horns  of  the  crescent,  i.  e., 
the  space  between  the  third  and  fifth  leaf  traces,  constitutes  the  so-called  "foliar 
gap"  which  faces  the  second  leaf  trace.  The  central  cells  of  the  young  stele  have 
already  begun  to  form  cambium,  which  in  the  older  stem  constitutes  such  a  char- 
acteristic feature  of  the  stele. 

Before  any  tracheary  tissue  is  formed  in  the  young  stele,  a  few  thick-walled 
cells  can  be  seen  in  the  outer  part  of  the  portion  of  the  stele  corresponding  to  the 
third  leaf  trace.  These  are  protophloem  cells,  and  similar  ones  are  developed  later 
in  the  younger  parts  of  the  stele.  The  first  tracheary  tissue  appears  in  the  region 
ofthe  steel  section  belonging  to  the  third  leaf  trace.     In  the  section  shown  (fig.  44,  C) 


A,  B,C.  The  young  vascula 

D.  Section  of  a  voiing  sporo 

stele  of  axis.      X75. 


bundles  of  : 
.hyie  of  B„tr 


there  are  three  groups  of  these  primary  tracheids,  separated  by  a  considerable  interval 
and  placed  at  the  extreme  inner  limit  of  the  young  stele.  In  the  older  portions  of 
the  bundle  the  number  of  these  increases  and  similar  ones  make  their  appearance 
in  the  next  younger  section  of  the  stele,  that  belonging  to  the  fourth  leaf.  Last  of 
all,  these  primary  tracheids  are  formed  in  the  younger  region  of  the  stele  and  new 
ones  arise  between  these  first-formed  ones,  so  that  there  is  developed  a  nearly 
complete  circle  of  tracheids  marking  the  inner  boundary  ofthe  tubular  stele. 

The  second  leaf  trace  approaches  nearer  and  nearer  the  two  horns  of  the 
crescentic  stele  section  as  it  is  followed  downward,  and  finally  joins  it,  filling  up 
the  gap  between  the  regions  belonging  to  the  third  and  fifth  leaf  traces.   Thus,  for  a 


64  THE    OPHIOGLOSSALES 

time  the  section  of  the  stele  appears  perfectly  circular  and  continues  downward 
until  it  reaches  the  next  leaf  trace,  which  marks  the  point  of  departure  of  the 
trace  of  the  cotyledon.  Except  for  the  greater  development  of  the  xylem,  which  is 
composed  of  two  to  three  concentric  rows  of  tracheids,  the  section  of  the  stele  in  this 
region  presents  much  the  same  appearance  that  it  does  in  the  younger  parts  nearer 
the  stem  apex.  The  outer  part  of  the  stele  at  this  point  shows  a  somewhat  broken 
row  of  thick-walled  bast  fibers  within  which  are  large  sieve  tubes.  The  cambium, 
lying  just  inside  the  phloem,  is  very  much  less  developed  in  the  basal  region  of  the 
stele  than  it  is  higher  up  and  can  scarcely  be  said  to  be  present.  The  stele  in  this 
region  of  the  stem  is  quite  similar  to  that  of  B.  lunarta,  figured  by  Poirault.  The 
endodermis  is  also  much  less  definite  than  it  is  later,  and  I  could  not  satisfy  myself 
that  there  was  in  B.  virgiiiianum  any  trace  of  the  inner  endodermis  which  Poirault 
states  is  present  in  the  basal  part  of  the  stem  in  B.  lunaria,  but  which  disappears 
later.  The  medullary  rays  also,  which  are  conspicuous  in  the  stele  of  the  older 
plant,  are  very  imperfectly  developed  in  this  basal  region. 

In  the  intermediate  region,  between  the  base  of  the  primary  root  and  the  trace 
from  the  cotyledon,  a  section  shows  a  thick  irregular  ring  of  tracheary  tissue  with 
no  clearly  developed  medullary  rays  (fig.  43,  L).  Indeed,  at  the  lowest  part  of  this 
region  the  tracheary  tissue  forms  an  almost  solid  core  with  only  a  small  amount  of 
parenchyma  interspersed,  thus  forming  an  inconspicuous  and  irregular  pith.  While 
the  endodermis  is  not  clearly  delimited,  some  of  the  cells  in  the  zone  of  tissue  sur- 
rounding the  stele  show  the  radial  thickenings  of  the  walls;  but  these  cells  are  not 
all  of  them  in  the  layer  immediately  adjoining  the  stele,  being  irregularly  disposed 
throughout  the  three  or  four  layers  of  cells  surrounding  the  stele.  As  sections  are 
examined  in  succession  upwards,  the  pith  becomes  better  defined.  Sections  taken 
downward  show  a  ring  of  tracheary  tissue  gradually  separating  into  the  two  or  three 
xylem  masses  of  the  primary  root. 

The  primary  root  in  the  sporophyte  which  has  just  been  described  was  diarch. 
The  stele  shows  a  very  evident  endodermis,  within  which  is  the  pericycle,  for  the 
most  part  composed  of  two  layers  of  cells.  The  xylems  are  composed  of  a  large 
group  of  tracheids,  of  which  the  two  or  three  smaller  ones  next  the  pericycle  repre- 
sent the  protoxylems.  Small,  deeply  staining  protophloem  elements  can  be  seen 
toward  the  outside  of  the  phloem,  and  within  these  are  the  other  phloem  elements, 
thick-walled  bast  fibers,  and  sieve  tubes.  The  rest  of  the  stele  is  composed  of  small, 
thin-walled  parenchyma  cells.  The  outer  region  of  the  root  is  made  up  of  somewhat 
compressed  cells  suggesting  the  periderm  cells  which  are  found  in  parts  of  the  older 
stem  and  which  are  also  present  in  the  cortex  of  the  later  roots.  This  outer  layer  of 
cells,  however,  shows  no  evidence  of  active  division. 

A  cross-section  of  the  petiole  of  the  cotyledon,  from  the  same  sporophyte,  taken 
at  a  point  some  distance  above  the  stipules,  shows  within  the  epidermis  about  three 
layers  of  parenchyma  cells  with  no  conspicuous  intercellular  spaces,  but  within 
these  are  several  very  large  lacunae,  separated  by  narrow  plates  of  tissue.  In  the 
center  of  the  section  are  seen  the  two  concentric  bundles  that  traverse  the  petiole. 
As  in  the  later  leaves  of  this  species,  these  bundles  are  truly  concentric,  thus  resem- 
bling those  of  the  Marattiace:f?  and  differing  from  the  collateral  bundles  of  Ophio- 
glossum  and  the  smaller  species  of  Botrychiuni.  The  phloem  is  better  developed 
upon  the  outer  side  and  small  protophloem  elements  can  be  seen  at  its  outer  limit, 
but  these  are  continued  partially  around  the  inner  side  of  the  bundle,  where  the 
xylem  is  separated  from  the  outside  by  about  two  layers  of  cells.  No  definite 
endodermis  can  be  made  out.  The  two  bundles  are  continued  up  to  the  base  of  the 
lamina,  where  one  of  them  passes  into  each  lateral  lobe  of  the  ternate  leaf.    One  of 


iiiK   'i()ii\(;  si'oKoi'in  1 1  65 

these  divides  and  i;ives  off  a  l.iaiuh  whieli  passes  int..  ilu-  teimmal  lolu-  . if  the  leat' 
(see  Jeffrey  1,  paj^e  2^). 

Ill  a  section  of  the  older  stiin,  .dioiit  where  the  tniiith  leaf  traei'  heeoines  joined 
to  the  rtfth  and  sixth,  the  section  of  the  stele  appeals  circular.  In  the  portion  hi- 
longinif  to  the  Hftli  leaf  trace  there  are  present  about  half  a  dozen  isolated  tracheids, 
arran<;ed  in  a  low,  while  in  the  sixth  trace  only  a  single  small  tracheid  is  developed, 
riu-  two  wlenis  of  the  fourth  leaf  trace  are  now  no  longer  distinguishable  and  the 
uocuh  pait  of  the  trace  has  the  form  of  an  irregular  row  on  the  inner  side  of  the 
trace  section,  and  is  continuous  with  the  xylems  of  the  fourth  and  Hfth  traces. 
l\\en  after  tin  fusion  of  rlu  se  three  traces  is  practically  complete,  it  is  still  evident 
that  the  ring-shaped  section  is  composed  of  three  parts,  the  break  between  the 
xylems  sht)wing  the  limits  of  the  three  component  leaf  traces.  With  the  increase  in 
the  development  of  the  .x\lem  ring  the  limits  of  the  individual  leaf  traces  are  finally 
completely  lost  and  the  section  of  the  stele  shows  a  thick  ring  of  the  tracheary  tissue 
interrupted  only  at  intervals  by  single  rows  of  parenchyma  cells  in  the  medullary  rays. 

Outside  the  ring  of  tracheids  there  can  be  seen  a  /one  of  narrow  cells  arranged 
in  radially  disposed  rows.  This  /one  constitutes  a  genuine  cambium,  precisely 
similar  in  appearance  to  that  found  in  the  stems  of  Conifers  and  Dicotyledons. 
Ibis  cambium  has  long  been  known  to  occur  in  the  older  sporophytcs  of  the  larger 
species  of  Botryc/iiitm,  and  Jeffrey  first  noted  it  in  the  young  sporophyte.  Ihe 
cambium  is  well  developed  in  the  leaf  trace  for  a  considerable  distance  above  its 
junction  with  the  central  stele. 

The  primary  tracheary  tissue  is  in  immediate  contact  with  the  pith.  Occa- 
sionally the  ring  of  tracheids  is  broken  by  a  single  parenchyma  cell.  Outside  the 
tracheary  ring  the  cells  are  arranged  in  radial  rows  and  in  these  the  formation  of 
the  walls  is  always  periclinal,  so  that  the  cambium  in  these  earlier  stages  presents  a 
very  characteristict  appearance.  The  rows  of  cambium  cells  continuous  with  the 
primary  parenchyma  cells  lying  between  the  tracheids  of  the  primary  row  do  not 
develop  tracheary  tissue,  but  remain  parenchymatous  and  thus  give  rise  to  the 
medullary  rays,  which  later  are  so  conspicuous. 

The  extreme  outer  portion  of  the  vascular  cylinder  is  composed  of  a  ring  of 
thick-walled  cells  which  are  probably  bast  fibers,  but  the  walls  of  these  do  not  stain 
strongly  with  safranine  and  are  hence  much  less  conspicuous  than  the  tracheids. 
These  may  possibly  be  considered  as  protophloem  elements  and  evidently  corre- 
spond to  the  zone  of  thick-walled  cells  figured  by  Poirault  for  B.  liinarui  (Poirault 
2,  fig.  1 1).  Just  outside  of  this  ring  of  thick-walled  cells  lies  the  endoderniis,  which 
has  not  as  yet  developed  the  characteristic  radial  thickenings  which  are  so  easily 
seen  in  the  older  parts  of  the  stele.  These  thick-walled  phloem  elements,  as  is  the 
case  with  the  protoxylems,  do  not  form  an  unbroken  ring,  but  are  interrupted  at  the 
junctions  of  the  confluent  leaf  traces  (fig.  44,  6'). 

In  the  older  bundle,  a  zone  of  large  cells,  the  \'oimg  sieve  tubes  nia\-  be  recog- 
nized l)ing  inside  the  ring  of  bast  fibers.  Inside  of  the  zone  of  sieve  tubes  lies 
the  cambium,  the  cells  of  which  gradually  pass  into  the  xylem,  to  which  constant 
but  slow  additions  are  made  from  the  cambium;  indeed,  Jeffrey  thinks  that  we  can 
not  speak  of  primary  wood.  He  considers  that  all  of  the  wood  owes  its  origin 
to  the  activity  of  the  cambium  ring.  The  radial  rows  of  secondary  wood  are  inter- 
rupted at  intervals  by  the  medullary  rays,  and  the  resemblance  of  the  stele  at  this 
stage  to  the  section  of  a  young  coniferous  stem  is  really  quite  remarkable.  The 
endoderniis  has  now  become  exceedingly  conspicuous,  as  the  lignificd  lateral  walls 
stain  very  strongly  with  safranine  and  stand  out  strongly  in  contrast  with  the  cells 
of  the  cortex  lying  outside  the  endoderniis.  1  he  inner  walls  of  the  endodermal 
5 


66  THK    OPHIOGLOSSALES 

cells  also  stain  more  or  less  strongly  with  the  safranine,  indicating  that  they  also  are 
partially  lignified. 

The  junction  of  the  second  leaf"  trace  with  the  central  stele  is  shown  in  Hg.  43, 
E,  F,  G,  and  similar  stages  in  the  fusion  of  the  first  leaf  trace  are  shown  in  fig. 
43,  H,  I.  The  junction  of  one  of  the  early  roots,  perhaps  the  third  root,  with  the 
central  stele  is  shown  in  fig.  43,  /.  At  the  level  where  the  second  leaf  trace  departs 
from  the  central  stele  the  .\ylem  ring  is  composed  of  about  three  rows  of  cells.  In 
both  this  second  leaf  trace  and  the  third  the  endodermis  is  very  conspicuous  upon  the 
outer  side  of  the  bundle,  but  is  not  developed  upon  its  inner  face.  As  the  trace 
approaches  the  central  cylinder  it  can  be  seen  that  the  endodermis  is  interrupted 
across  the  leaf  gap,  but  as  the  leaf  trace  approaches,  endodermal  cells  are  developed 
between  the  endodermis  of  the  central  cylinder  and  that  of  the  leaf  trace.  This 
union  takes  place  first  upon  one  side,  the  gap  being  closed  sooner  on  one  side  than 
the  other,  but  later  a  similar  process  takes  place  on  the  other  side  of  the  leaf  trace 
and  the  closing  of  the  gap  is  complete,  the  endodermis  now  being  continued  without 
interruption  around  the  whole  of  the  circular  section.  The  leaf  trace  where  it  joins 
the  central  cylinder  is  exactly  like  it  in  size  and  structure;  indeed,  it  is  nothing  more 
than  a  sector  of  the  hollow  cylindrical  stele,  which  is  evidently  built  up  exclusively 
of  these  fused  leaf  traces.  There  is  no  vestige  of  a«v  tissue  in  the  stele  which  is  not 
referable  to  the  bases  of  the  leaf  traces  themselves.  This  becomes  very  evident  when 
the  structure  of  the  leaf  trace  is  examined  before  it  closes  the  gap  where  it  joins  the 
central  stele. 

An  examination  of  the  outer  tissues  of  the  older  portions  of  the  stem  (fig.  42) 
show  that  at  certain  points  there  is  a  conspicuous  border  of  periderm  (per),  forming 
a  layer  some  four  or  five  cells  deep.  This  border  of  periderm  occupies  about  a  third 
of  the  circumference  of  the  section  and  marks  the  position  of  an  old  leaf  base  which 
has  fallen  away.  According  to  Jeffrey,  this  periderm  is  an  "abciss"  layer  and 
results  in  the  cutting  off  of  the  old  leaf  bases.  He  suggests  that  the  layer  of  cork 
cells  developed  from  the  periderm  closes  the  scar  left  by  the  dead  leaf  and  may  be 
efficacious  in  preventing  infection  from  fungi  in  the  soil.  The  presence  of  a  periderm 
in  the  outer  cortex  of  the  Ophioglossaceae  was  first  pointed  out  by  Russow  (Russow 
1),  and  was  afterward  confirmed  by  Holle  (Holle  I).  The  periderm  in  B.  vtrgin- 
taniim  is  made  up  of  the  usual  radially  arranged  rows  of  cells  (fig.  42,  per). 

All  of  the  tracheary  tissue  in  the  young  sporophyte  is  composed  of  rather  short, 
reticulately  marked  tracheids.  The  secondary  tracheids  increase  in  size  and  the 
thickened  bars  on  their  walls  become  broader,  so  that  the  larger  elements  have  their 
walls  pitted  rather  than  reticulately  marked,  and  these  pits,  especially  in  the  older 
plant,  are  of  the  bordered  type,  not  very  unlike  the  round  bordered  pits  found  in 
the  wood  of  Conifers. 

The  elongated  thick-walled  elements  in  the  outer  part  of  the  phloem  are 
probably  bast  fibers.  In  the  older  part  of  the  bundle  thesje  stain  quite  strongly  with 
safranine  and  show  irregular  pits  upon  their  walls.  The  sieve  tubes  do  not  show  at 
all  clearly  in  sections  mounted  in  balsam.  They  are  evidently  large,  but  the  char- 
acteristic dotted  sieve  areas  can  not  be  made  out  and  no  special  study  was  made  of 
these.  Between  the  large  secondary  tracheids  and  the  phloem  are  the  narrow,  thin- 
walled  cambium  cells.  These  probably  contribute  only  to  the  wood,  and  there  is 
no  secondary  phloem. 


INI-  \(»i  \(;  si'okonn  I ;  oi   iii  i.mi.n  niosi  \cins. 

I  lu'  ()iil\  iKiDimt  rli:ir  li;is  \\t  Ihim  piihlislucl  of  the  \(iuni;  s|)()rii|)hvfi'  of" 
Helnunthost(hh\s  is  rli:it  of  I.aiig  {Lang  I),  wlio  examined  at  sonic  length  the 
vascular  system  in  the  \(iiinii  spoiophyte.  Lang  states  that  the  young  sporophyte 
of  Hflniinthosttii  /i\s  develops  its  first  leaf  as  a  large  teinate  foliage  leaf,  and  when  I 
first  examined  the  young  plants  which  were  collected  in  Ceylon  I  reached  the  same 
conclusion;  hut  on  making  sections  of"  the  young  sporophyte  it  was  found  that  in 
all  of  the  young  plants  that  were  sectioned  the  supposed  cotyledon  was  really  the 
second  leaf,  the  cotyleilon  itself  hcing  rudimentary  and  forming  an  inconspicuous 
papilla  at  the  base  of  the  second  leaf,  which  was  the  first  to  develop  a  functional 
lamina.  Further  examination  of  a  number  of  other  specimens  showed  that  this 
rudimentary  cotyledon  was  also  present  and  it  is  probable  that  the  cotyledon  in 
Hcluiinthostaihys,  as  in  Botrychiuui  huiaria  and  Ophioglossum  vtilgatiinu  is  always 
a  rudimentary  organ  which  never  appears  above  the  ground. 

Fhe  youngest  sporophytes  oi  Helminthost(ich\s  which  were  found  alread\-  had 
the  second  leaf  well  developed  and  the  first  root  had  emerged.  The  ternate  second 
leaf  (fig.  lo,  C)  shows  clearly  that  the  ternate  form  is  the  result  of  an  unequal  dichot- 
omy, such  as  is  common  in  the  early  leaves  of  many  ferns.  The  second  leaf  of 
Helmnithostachys  closely  resembles  the  cotyledon  of  Rotrychnim  vtrgmianutn  and, 
like  that,  usually  possesses  two  vascular  bundles  extending  through  the  long,  slender 
petiole.  At  the  base  of  the  leaf  there  is  a  conspicuous  stipular  sheath  which 
completely  incloses  the  next  younger  leaf,  as  it  does  in  Botrychium  liinaria.  The  two 
bundles  of  the  petiole  contribute  to  the  two  lateral  lobes  of  the  leaf  as  they  do  in  the 
cotyledon  of  Botrychium  virgiuianiim,  and  one  of  these,  forking  again,  gives  rise 
to  the  terminal  lobe  and  smaller  lateral  lobe.  The  venation  of  the  second  leaf, 
especially  in  its  younger  stages,  is  almost  perfectly  dichotomous  and  is  more  like 
the  venation  in  the  leaves  of  Botrychium  lunaria  than  that  of  5.  virginianum.  With 
the  enlargement  of  the  leaf  segments  the  venation  more  nearly  approaches  the 
pinnate  arrangement  found  in  the  later  leaves. 

While  the  young  sporophyte  in  Helminthostachys  in  its  earliest  stages  shows  a 
general  resemblance  to  that  of  Botrychium  virginianum,  a  difference  is  very  soon 
noted.  The  young  plant,  very  soon  after  the  formation  of  the  cotyledon,  develops 
a  conspicuous  internode  between  the  cotyledon  and  the  root,  and  the  stem  rapidly 
elongates  as  the  sporophyte  grows,  so  that  it  soon  shows  the  characteristic  elongated 
rhizome  of  the  older  sporophyte. 

Unfortunately  I  was  unable  to  secure  any  very  young  sporophytes,  my  youngest 
specimens  already  having  the  second  leaf  nearly  fully  developed.  According  to 
Lang,  the  arrangement  of  the  primary  organs  of  the  young  sporophyte  is  the  same 
as  in  B.  virginianum,  but  I  could  make  no  study  of  the  origin  of  the  vascular  system 
in~the  sporophyte  before  the  first  leaf  and  root  had  emerged  from  the  prothallium. 

To  judge  from  longitudinal  sections  of  the  youngest  plants  obtained,  the 
relation  of  the  first  leaf  and  root  is  the  same  as  in  Botrychium  virginianum  and  the 
base  of  the  young  sporophyte  closely  resembles  that  of  the  latter.  As  in  Botrxchium, 
the  foot  is  very  large  and  conspicuous,  forming  a  large,  hemispherical  body  sur- 
rounded by  the  prothallial  tissue.  The  large  primary  root  grows  out  at  right  angles 
to  the  foot  and  is  continued  into  the  axis  of  the  sporophyte,  which  grows  up  verti- 
cally. None  of  the  specimens  were  young  enough  to  show  the  relation  of  the  stem 
apex  to  the  first  leaf  and  root,  as  in  the  \-oungest  specinu-iis  the  axis  hatl  alriad\' 
begun  to  elongate  and  an  cvidcnr  iiucrnodc  was  forimd  between  tiie  hasi-  of  the 
first  leaf  and  the  root. 


68 


THE    OPHIOGLOSSALEf 


The  longitudinal  section  of  the  young  sporophyte  at  this  time  shows  that  the 
thick  stele  of  the  root  bends  upward  and  is  continued  into  the  axis,  which  already 
is  a  good  deal  elongated  and  has  carried  up  the  young  leaves,  which  are  separated 
from  each  other  by  conspicuous  internodes.  The  young  sporophyte  at  this  stage 
thus  differs  strikingly  from  the  corresponding  stages  in  Ophioglossiim  and  Botrych- 
iiim,  with  their  very  closely  crowded  leaves  with  no  appieciable  internodes  between 
them  (fig.  46). 

A  single  stele  extends  through  the  axis  from  its  junction  with  the  root  stele  and 
forks  below  the  insertion  of  the  rudimentary  first  leaf,  one  branch  passing  into  the 
cotyledon,  the  other  continuing  upward  and  forming  the  trace  for  the  second  leaf, 
at  whose  base  is  seated  the  apical  bud. 

Whether  in  the  younger  stages,  before  the  development  of  the  second  leaf,  the 
vascular  system  of  the  young  spoidph\tL-  would  show  the  same  relations  of  the  steles 
of  the  root  and  cotyledon,  as  in  /io/rvi  /'///"/, n^nuiins  to  be  seen;  but  from  the  general 
similarity  in  the  structure  of  the  \()ung\sponiph\tes  of  the  two  this  is  quite  likely; 

yet  it  is  possible  that  the  stem  apex  is 
more  prominent  in  the  early  stages  of 
Helminthostachvs  and  part  of  the  stele 
which  is  found  in  the  elongated  stem 
may  be  of  cauline  origin,  although  this 
is  hardly  indicated  by  the  condition  of 
things  in  the  apical  meristem  of  the 
youngest  sporophytes  that  were  ex- 
amined. 

The  foot  is  composed  of  large- 
celled,  thin-walled  parenchyma,  with 
no  noticeable  differences  between  the 
inner  tissue  and  that  of  the  periphery. 
The  stele  of  the  root  is  continued  up- 
ward without  interruption  into  that  of 
the  shoot  (fig.  46,  B).  Probably  at  an 
earlier  period  there  would  have  been, 
as  in  Botrychium,  simply  the  continu- 
ous stele  of  the  root  and  cotyledon. 
At  the  junction  of  the  root  stele  with 
that  of  the  axis  there  is  a  marked  en- 
largement, and  the  short,  somewhat  ir- 
regular tracheids  are  decidedly  broader 
than  those  either  in  the  root  or  in  the  portion  of  the  stele  above  the  junction.  The 
tracheids  toward  the  outside  of  the  central  region  are  slender  and  have  delicate 
reticulations,  which  closely  approximate  the  form  of  true  spiral  thickenings.  These 
are  the  protoxylem  elements  and  can  be  traced  upward  and  downward  into  the 
stem  and  root,  respectively.  The  secondary  tracheary  tissue  is  marked  by  broad, 
reticulate  thickenings,  and  these  in  the  largest  tracheids  are  replaced  by  conspicu- 
ous oval  or  nearly  round  bordered  pits,  very  much  like  those  which  are  found  in  Bo- 
trychium (fig.  46,  £). 

Above  the  base  of  the  root  there  is  a  long  internode  below  the  cotyledon,  and 
through  this  runs  the  single  axial  stele.  On  the  same  side  of  the  axis  as  the  primary 
root  may  be  seen  the  cotyledon,  which  closely  resembles  in  form  the  young  cotyledon 
of  Botrychium  virginianum,  but  instead  of  developing  into  a  functional  leaf  it  is 
arrested  in  its  growth  before  the  lamina  is  fully  developed.    As  in  the  cotyledon  of 


L  Young   sporophyte   of    Hehnitilhostachv 
phyte,  pr.   ror,  cotyledon;  r',r^,  first 
i.  Le.lf  from  an  older  sporophyte.     Xl. 


attached    to  gameto 


TIIK     VOINC    SPOKOI'inTI-  69 

Botiycliiniii  vivgnuanuiu,  the  lamina,  wliicli  althouyli  \li)-  j;ii.atl\-  iliIullcI  iilact- 
theless  is  present,  is  bent  over  sharply  against  the  stout  petiole,  which  is  strongly 
convex  on  its  adaxial  side.  In  the  specimen  figured  there  was  nf)  trace  of  a  stipular 
sheath  developed  in  the  cotyledon,  but  sometimes  this  is  very  well  developed, 
although  the  ujiper  part  of  the  cotyledon  remains  quite  rudimentary.  The  little 
cotyledon  has  the  rudimentary  lamina  distinctly  ternate  in  outline  and  very  much 
resembles  some  of  the  rudimentary  early  leaves  found  in  liotrychiuni  lunaria,  as 
figured  by  Bruchmann.  A  single  vascular  bundle  extends  through  the  petiole  of  the 
cotyledon,  nearly  to  the  base  of  the  lamina,  but  except  in  the  basal  region  the 
development  of  the  xylem  is  niL-.ch  reduced  and  is  entirely  lacking  before  the  lamina 
is  reached.  The  bundle  of  the  cotyledon,  where  it  bends  at  the  base  into  the  inter- 
node,  is  nearly  as  well  developed  as  the  bundle  of  the  second  mttriiode  which 
separates  from  the  former  just  below  the  insertion  of  the  cotyledon.  ( )n  tin-  ()|)|iosirf 
side  of  the  second  internode  from  the  C(ir\ledon,  and  exttiuling  downwaiil  tliinnuh 
x\w  Hrsr  internode  for  a  short  distance  below  the  level  of  the  eon  ledon.  tlieie  is  seen 


F.o.  46. 

A,  B.  Two  longitudinal  sections  of  a  young  sporophyte  of  H^/mm/Ao5Mc/;vj;  /)r,  gametophyti'.     X6. 
C.  Upper  part  of  same,  more  enlarged;   b,  terminal  bud;    col,  cotyledon;    i,  lacuna  in  first  internode. 
O.  Apical  region.    /^,  third  leaf;   sc,  epidermal  scales.     X140. 
E.  Tracheids  showing  bordered  pits  and  thickened  bars.     X320. 

in  the  specimen  figured  a  large  lacuna,  separated  from  the  outside  of  the  internode 
by  about  half  a  dozen  layers  of  cells  and  on  its  inner  side  from  the  endodermis  of  the 
stele  b\  two  or  three  layers  of  cells.  This  lacuna,  as  Lang  pointed  out,  is  not  always 
present.  At  the  upper  end  of  the  second  internode  can  be  seen  the  base  of  the  second 
leaf,  the  stipular  sheath  of  which  incloses  the  \()ung  bud  at  the  summit  of  the  axis. 

On  its  inner  (dorsal)  side  the  terminal  bud  shows  the  young  third  leaf,  opposite 
which  is  the  section  of  the  ridge  surrounding  the  small  free  surface  of  the  stem  apex, 
ver\-  much  like  the  condition  in  the  \-oung  bud  of  Opbioglossuni  tnohucatuim. 
The  form  of  the  young  leaf  at  this  stage  is  more  like  that  of  BotrYcli/iini  liuuiriu  than 
that  of  B.  v'lrg'niiantitn.  The  young  leaf  is  a  blunt  cone  with  a  marked  projection 
on  its  inner  side,  extending  over  the  apex  of  the  stem  and  marking  the  beginning 
of  the  stipular  sheath,  which  is  entire  as  in  B.  hninnu,  and  not  di\iileil  into  two  fite 
stipules  as  in  B.  virgnuniiiini  (fig.  4'i,  /)).  .\  conspicuous  strand  of  |ii(icambium 
extends  into  the  leaf  and  joins  the  trace  of  the  second  leaf.  As  in  Bntixilninn  and 
Opliioglos.uim,  the  stele  of  the  internode  does  not  extend  upwartl  be\()nil  the  base  of 
the  youngest  leaf  and  there  is  no  indication  that  it  derives  any  of  its  tissues  directly 


70 


THE    OPHIOGLOSSALES 


from  the  apical  meristem  of  the  shoot.  Fhe  latter,  as  in  the  other  Ophioglossaceae, 
shows  a  large  single  initial  cell,  which  in  section  closely  resembles  that  of  Ophio- 
glossum  mohiccaniim,  having  a  broadly  truncate  base  and  being  narrower  above 
(fig.  46,  D).  The  apical  meristem  is  of  very  limited  extent  and  segmentation  of  the 
apical  cell  is  probably  very  slow.  The  second  root,  which  in  the  case  under  con- 
sideration arose  near  the  base  of  the  third  leaf,  is  here  very  conspicuous  and  its  stele 
joins  that  of  the  third  leaf  near  the  base  of  the  internode.  The  young  leaf  and  root, 
with  the  inconspicuous  stem  between  them,  have  very  much  the  appearance  of  a 
bud  at  the  base  of  the  second  leaf.  The  apex  of  the  very  young  leaf  grows  from  the 
conspicuous  single  apical  cell  (fig.  46,  D).  This  appears  triangular  in  longitudinal 
section  and  shows  regular  segmentation.  The  stele  of  the  young  leaf  can  be  traced 
up  to  the  inner  cells,  cut  off  from  the  lateral  segments  of  the  apical  cell. 

The  apical  cell  of  the  stem  is  quite  large  and,  as  we  have  seen,  is  truncate  below, 
as  it  is  in  Ophioglossum.  Seen  in  its  transverse  section  it  is  triangular,  so  that  its 
form  is  really  that  of  a  three-sided  prism.  Both  lateral  and  basal  segments  are  cut 
off  from  it,  but  only  the  youngest  segments  can  be  clearly  distinguished.  Below  the 
apical  cell  there  is  only  a  very  small  amount  of  tissue  between  the  apex  of  the  shoot 
and  the  point  of  the  junction  of  the  two  leaf  traces  and  the  stele  of  the  second  root. 
This  junction  is  marked  by  the  presence  of  very  irregular  reticulate  tracheids  (fig. 
46,  D,  tr).    The  tissues  on  the  upper  side  of  the  root  stele  extend  to  within  a  few  cells 

of  the  stem  apex  and  may  possibly 
represent  a  portion  of  the  internodal 
stele  that  is  not  connected  with  the 
leaf  trace,  but  a  study  of  later  stages 
does  not  support  this  view,  and  it 
is  almost  certain  that  this  youngest 
tracheary  tissue  is  the  beginning  of 
the  next  leaf  trace. 

From  the  very  first,  as  Lang 
pointed  out,  the  shoot  is  perfectly 
dorsiventral,  although  at  first  it  grows 
vertically  upward.  The  leaves  are  all 
borne  upon  the  dorsal  side,  while  the 
roots  invariably  arise  upon  the  ven- 
tral side. 

The  apex  of  the  young  root, 
which  in  this  case  is  on  the  point  of 
emerging,  is  occupied  by  a  conspicu- 
ous triangular  apical  cell,  the  segmen- 
tation of  which  closely  resembles  that 
of  the  root  o( Botrychntni.  At  first  the  root  cap  is  mainly  derived  directly  from  the 
outer  segments  of  the  apical  cell.  These  segments  undergo  periclinal  as  well  as 
anticlinal  divisions  and  the  inner  layers  of  the  root  cap  (which  at  this  stage  is  rela- 
tively thick)  show  a  fairly  regular  stratification.  The  outer  cells  of  the  root  cap  are 
a  good  deal  elongated,  so  that  the  free  end  of  the  root  is  decidedly  pointed.  At  this 
time,  except  for  the  irregular  conjunctive  tracheids  at  the  base,  no  permanent  tissue 
can  be  seen  in  the  stele  of  the  young  root. 

In  the  cross-sections  of  a  young  sporophyte  of  about  the  same  age  the  third  leaf 
was  rather  further  developed  and  the  young  fourth  leaf  could  be  seen,  but  the  second 
root  was  not  so  far  advanced,  or  it  may  be  that  the  root  at  the  base  of  the  third  leaf 
was  the  third  root  and  not  the  second.    The  single  apical  cell,  which  was  so  prominent 


ng  sporophyte  of  Hetminthos- 
;  Z'',  second  leaf.    X65. 


B.  Section  passing  through  I 

C.  Stem  apex.     X200. 


THE    YOUNG    SPOROI'HYTF 


71 


in  the  very  young  leaf,  can  no  longer  be  recognized  and  the  lamina  is  divided  into 
two  nearly  equal  lobes,  of  which  one  is  lateral  with  reference  to  the  other,  but  these 
two  lobes  probably  arise  as  a  result  of  the  dichotomy  of  the  original  apex.  A  group 
of  narrow  marginal  cells  somewhat  to  one  side  of  the  terminal  lobe  evidently  consti- 
tuted a  meristem  tissue,  and  this  was  preparing  for  the  second  dichotomy,  by  which 
the  ternate  form  of  the  young  leaf  is  established.  The  branching  of  the  lamina  at 
this  early  period  therefore  appears  to  be  the  result  of  an  unequal  dichotomy,  as  it  is 
in  the  first  foliage  leaf.  The  vascular  bundles  from  each  of  the  two  primary  leaf  seg- 
ments were  just  beginning  to  be  recognizable  and  join  into  one  at  the  base  of  the 
lamina.  Surrounding  the  leaf  is  the  sheath  developed  from  the  base  of  the  second 
leaf.  This  sheath  in  the  section  appears  as  a  closed  ring  some  two  or  three  cells  in 
thickness  and  looking  very  much  like  the  sheath  of  Ophwglossiim.  \  he  top  of  the 
conical  sheath  is  closed  and  does  not  show  the  pore  found  in  Ophioglossuni.  The 
sheath  becomes  thicker  lower  down,  where  four  rows  of  cells  show  in  the  section. 
Between  the  inclosed  leaf  and  the  surrounding  sheath  in  the  lower  portion  (fig.  49,  B) 
may  be  seen  the  section  of  flattened  scales  (sc)  which  grow  from  the  base  of  the  leaf 


and  from  the  tissue  immediately  about  the  stem  apex.  At  its  base  the  sheath  of 
the  third  leaf  is  already  completely  developed  and  surrounds  the  young  fourth  leaf 
(/*),  which  in  this  section  was  cut  horizontally  and  shows  plainly  its  large  apical  cell. 
The  stem  apex,  which  lies  directly  below  the  younger  leaf,  was  cut  obliquely  in  this 
series  and  did  not  show  the  form  of  the  apical  cell  plainly,  but  in  a  young  plant  of 
about  the  same  age  (fig.  47,  6")  the  apical  cell  showed  that  it  was  regularl}-  trian- 
gular in  form,  seen  in  cross-section. 

At  the  level  of  the  stem  apex  the  second  leaf  shows  a  single  vascular  bundle 
which  may  be  continued  undivided  upward,  or  it  may  divide  into  two  bundles  in  the 
petiole.  In  regard  to  the  structure  of  the  petiole,  therefore,  Helniintliostnchys  is  to 
some  degree  intermediate  between  Botryrliium  and  Ophioglossum.  The  young  trace 
of  the  third  leaf  can  be  seen  at  this  level  as  an  oval  mass  of  undifferentiated  cam- 
bium. Immediately  below  the  stem  apex  the  cells  are  smaller  than  is  the  case  in 
the  young  sporophyte  of  Botrychium,  but  one  can  not  make  out  the  beginning  of  a 
central  procambium  cylinder.  The  smaller  cells  in  the  region  immediately  underlying 
the  stem  apex  may  be  explained  by  the  fact  that  in  these  voung  plants  there  is  no 
pith  developed  within  the  axial  stele  as  there  is  later  on.    The  youngest  root  in  this 


72 


THE    OPHIOGLOSSALES 


specimen  was  less  developed  than  that  in  the  specimen  that  we  have  just  described. 
This  3'oungest  root  was  cut  obhquely,  but  at  its  base  there  could  be  seen  the  undif- 
ferentiated mass  of  procambium  forming  its  stele,  and  the  apex  showed  the  tetra- 
hedral  apical  cell,  presenting  much  the  same  form  as  the  longitudinal  section.  The 
apical  portion  of  the  young  root  was  somewhat  shrunken  away  from  the  surrounding 
tissue,  so  that  there  was  ajjvery  evident  space  surrounding  it.  Whether  or  not  this 
was  the  result  of  artificial  shrinkage  was  not  certain. 

Below  the  terminal  bud  the  third  leaf  trace  proceeds  downward  into  the  inter- 
node  below,  and  the  tracheary  tissue,  which  is  just  beginning  to  develop  in  the  bud 
region,  increases  rapidly  in  amount  and  forms  a  central  mass  of  wood  which  does 


c 

D.  Shows  the  narrow  pit,  y^  bet 
G-J.  Show  only  the  vascular  bundles. 

not  appear  solid,  but  is  made  up  of  two  groups  of  tracheids,  of  which  the  one  nearest 
the  second  leaf  trace  has  the  larger  tracheids.  At  this  stage  the  bundle  somewhat 
resembles  the  section  of  a  diarch  root.  Only  a  little  further  down  the  two  xylem 
masses  are  joined  by  the  development  of  tracheids  in  the  middle  of  the  bundle, 
which  thus  comes  to  have  a  solid  xylem  core.  In  the  section  figured  there  may  be 
seen  a  single  small  isolated  tracheid  on  the  side  turned  toward  the  second  leaf  trace, 
which  has  now  approached  so  close  to  the  central  bundle  as  to  touch  it  (fig.  50,  A). 
The  central  bundle  in  the  internode  at  this  point  is  beyond  question  the  leaf  trace  for 
the  third  leaf.  There  is  no  difficulty  in  tracing  its  progress  upward  to  where  it  enters 
the  leaf  and  there  is  no  sign  of  any  addition  to  it  from  tissue  lying  outside  the 
original  leaf  trace.  The  central  stele  of  the  upper  part  of  the  second  internode  is 
throughout  nothing  more  than  the  basal  portion  of  the  leaf  trace  from  the  third  leaf. 
At  this  point  it  is  concentric  in  structure.  Surrounding  the  solid  .xylem  core  can  be 
seen  about  three  rows  of  phloem  cells,  some  of  the  outer  ones  being  small  protophloem 
elements.  The  large  ones  lying  inside  are  presumably  sieve  tubes.  A  single  layer 
of  rather  large  pericycle  cells  separates  the  phloem  from  the  large  endodermal  cells, 
which  begin  to  show  very  conspicuously  lignified  radial  thickenings,  especially  on 
the  side  of  the  bundle  adjacent  to  the  second  leaf  trace.  The  section  of  the  second 
leaf  trace  is  somewhat  extended  transversely  and  the  xylem  band  is  composed  of 
about  a  dozen  tracheids.  In  the  mid  region  of  the  section  the  xylem  is  separated 
from  the  inner  side  of  the  bundle  by  a  single  layer  of  cells,  possibly  sieve  tubes,  but 
at  one  point  the  xylem  is  in  contact  with  the  pericycle,  which  is  only  imperfectly 
developed  and  wanting  at  certain  points.  Upon  the  dorsal  side  the  phloem  may 
be  in  direct  contact  with  the  endodermis,  which  is  quite  wanting  at  this  point  upon 
the  ventral  side  of  the  bundle.  Higher  up,  where  the  trace  is  quite  free,  the  endo- 
dermis extends  completely  around  it.     While  the  second  leaf  trace,  therefore,  may 


73 


be  said  to  be  concentric,  it  neveitbeless  a|)[ii()acbe.s  closel\'  tbi  collateiai  tv|)e  of" 
the  other  ( )phioglos.sace:L'. 

The  fusion  of  the  two  leaf  traces  to  form  the  sin<>;le  axial  binulle  in  the  basal 
part  of  the  internode  is  very  nuich  like  that  found  in  the  young  sporophyte  of /io- 
trycluiini  (fig.  49,  D,  F).  l"he  endoderniis  of  the  two  bundles  becomes  continuous 
and  there  may  be  seen  intermediate  stages  of  a  single  bundle,  oval  in  section,  but 
with  two  conspicuous  xylems,  separated  by  the  mass  of  large,  thin-walled  tissue 
which  gradually  disappears  as  the  bundle  is  followed  downward;  and  finally,  in  the 
lower  part  of  the  internode,  the  section  of  the  stele  appears  quite  circular,  the  center 
being  occupied  by  the  solid  xylem  formed  by  the  complete  coalescence  of  the  xylems 
of  the  fused  leaf  traces  (fig.  49,  J).  The  arrangement  of  the  phloem,  pericycle,  and 
endoderniis  is  the  same 
as  in  the  single  leaf  trace  '^  ')~^X^^ 

in  the  upper  region  of  the  \/\1yh-( 

niternocle.  <  \J'-0': {,.->(:%% 

The  base  of  the  stip- 
ular  sheath  can  be  fol- 
lowed downward  to  about 
the  level  where  the  two 
leaf  traces  begin  to  coal- 
esce. Its  anterior  free 
portion,  betwten  which 
and  the  internode  is  a 
narrow  slit,  finally  be- 
comes quite  free  and  its 
section  is  visible  as  an 
oblong  mass  of  cells  lying 
quite  separate  from  the 
section   of  the  internode. 

Longitudinal  sections 

of  a  somewhat  older  sporophyte  are  shown  in  fig.  48,  A,  B;  the  third  leaf  is  pretty 
well  developed,  with  the  stipular  sheath  completely  overarching  the  stem  apex  and 
the  fourth  leaf,  which  already  is  conspicuous.  The  third  leaf  is  still  completely 
covered  by  the  large  stipular  sheath  of  the  second  leaf,  which  apparently  forms  a 
closed  cavity;  but  an  examination  of  the  adjoining  sections  showed  that  the  ante- 
rior margin  of  the  sheath  is  quite  free  in  front  and  that  there  is  a  narrow  cleft 
between  it  and  the  internode.  Ihe  real  nature  of  the  sheath  and  its  relation  to  the 
leaf  base  is  very  clearly  shown  in  the  nuilian  section  ot  the  terminal  bud  from  an 
older  plant  (fig.  48,  Cy  D),  and  the  resemblance  to  the  terminal  bud  of  Botrvr/mitu 
linifin'ri,  except  for  the  dorsiventral  arrangement  of  the  parts,  is  most  striking.  This 
is  equally  marked  in  the  adult  sporoph\te,  as  Farmer  has  already  pointed  out. 

rile  specimen  under  consideration  diffeied  somewhat  from  the  yoimger  one 
that  was  descrilnd  in  the  relation  of  tht-  \-oung  organ.s.  The  cotyledon  was  better 
developed  and  although  the  lamina  was  rudimentary  the  stipular  sheath  was  large 
and  inclosed  the  base  of  the  second  leaf,  while  in  the  younger  specimen  discussed 
no  sheath  was  developed  at  the  base  of  the  cot\ledon.  There  was  a  diflVrent  rela- 
tion of  the  r(M)ts  also,  pidhahK  associated  with  the  greater  (livelo|inuin  of  the 
cot\'ledoii  in  rile  specimen  under  consideration.  The  second  root,  instead  of  being 
formed  at  the  base  of  the  third  leaf  in  the  terminal  bud,  was  developed  a  short  dis- 
tance above  the  cotyledon,  near  the  base  of  the  second  leaf,  while  in  the  \-oungei 
specimen  no  root  was  developed  above  the  primary  root  until  the  third  leaf  had 


74  THE    OPHIOGLOSSALES 

begun  to  develop;  but  this  second  root  developed  much  earlier  in  its  relation  to  the 
development  of  the  next  leaf  than  was  usually  the  case. 

In  the  present  plant  the  root  corresponding  to  the  third  leaf,  which  was  the 
third  root  in  this  case,  was  in  a  very  early  stage  of  development  and  had  not  begun 
to  elongate  at  all.  The  third  leaf  in  median  section  was  already  pretty  well  advanced 
and  the  apical  portion  was  very  strongly  incurved,  as  it  is  in  the  young  leaves  of 
Botrychium  virginiatium,  which  it  resembles  more  than  it  does  that  of  B.  lutiaria, 
and  it  also  suggests  the  form  of  the  young  leaves  in  the  Marattiaceae.  The  basal 
part  of  the  young  leaf,  however,  is  exactly  like  that  of  B.  lunarta.  The  stipular 
sheath  forms  a  thick  body,  projecting  forward  and  about  equal  in  height  to  half  the 
total  length  of  the  young  leaf.  It  is  strongly  concave  below,  and  the  next  leaf  is 
fitted  into  the  cavity  (fig.  48,  C).  The  forward  margin  extends  downward  as  a  sort 
of  lip  which  elongates  rapidly  and  keeps  pace  with  the  growth  of  the  young  leaf 
inclosed  within  it,  and  this  is  completely  concealed  until  it  has  reached  a  large  size. 
The  sheath  finally  forms  a  long,  conical  protuberance  at  the  base  of  the  leaf  to  which 
it  belongs. 

The  cavity  below  the  sheath  is  extended  backward,  so  that  the  base  of  the  leaf 
is  hollowed  out  in  front  and  in  section  appears  much  narrower  than  the  part  of  the 
petiole  above  the  insertion  of  the  sheath;  this  brings  the  stele  of  the  leaf  very  close 
to  the  epidermis  at  this  point.  The  narrow  cleft  thus  formed  between  the  posterior 
wall  of  the  stipular  cavity  and  the  petiole  of  the  leaf  in  front  is  the  "canal,"  which 
Gwynne-Vaughn  described  as  occurring  at  the  base  of  the  petiole  of  the  older  plant 
and  opening  above  the  insertion  of  the  stipule.  These  canals  are  easily  seen  in  longi- 
tudinal sections  of  the  young  bud  (fig.  48,  B)  and  it  is  very  clear  that  they  are,  in  truth, 
nothing  but  the  narrow  spaces  between  the  bases  of  the  adjacent  leaves.  Gwynne- 
Vaughn's  statement  that  they  open  above  the  insertion  of  the  stipules  is  incorrect 
unless  the  stipules  of  a  given  leaf  are  considered  to  be  derived  from  the  sheath  sur- 
rounding the  base  of  the  leaf,  this  sheath  properly  belonging  to  the  next  older  leaf. 
This  canal  can  be  seen  as  a  narrow  slit  in  the  young  leaf,  extending  below  the  inser- 
tion of  the  next  younger  one,  the  young  stele  of  the  leaf  being  separated  from  the 
epidermis  at  this  point  by  only  about  three  rows  of  cells. 

The  stele  of  the  young  leaf  can  be  traced  nearly  to  its  tip,  and  then  continues 
downward  toward  the  inner  side  of  the  leaf  into  the  internode,  below  where  it  joins 
the  young  stele  belonging  to  the  next  younger  leaf. 

As  in  the  younger  sporophyte,  the  stem  apex  is  of  very  limited  extent  and  the 
apical  cell  shows  the  same  form.  In  the  section  figured  (fig  48,  C)  the  youngest  leaf 
is  cut  almost  m  a  median  plane  and  though  externally  no  differentiation  is  visible  the 
young  stele  is  already  conspicuous  and  can  be  followed  down  without  difficulty. 
Passing  on  one  side  of  the  stem  apex  and  above  the  leaf  trace,  there  is  no  evidence  of 
procambium  in  the  apical  region  of  the  stem.  In  the  young  sporophyte,  therefore,  it 
is  perfectly  certain  that  no  cauline  stele  is  present.  Farmer  (Farmer  2)  states  that 
in  the  older  sporophyte  the  stele  can  be  traced  above  the  insertion  of  the  youngest 
leaves,  but  we  believe  a  careful  study  of  this  point  in  the  older  plant  would  show,  as 
in  the  younger  one,  that  the  stele  is  developed  in  the  young  leaf  at  an  exceedingly 
early  period  and  that  the  stele  of  the  internode  is  composed  entirely  of  leaf  and  root 
traces.  The  procambium  tissue  developed  on  the  ventral  side  of  the  stele  near  the 
apex  can  be  shown,  by  a  study  of  its  transverse  sections,  to  be  due  entirely  to  tissue 
derived  from  the  leaf  traces,  which  are  extended  downward  until  they  meet  on  the 
ventral  side  of  the  internode. 

Near  the  stem  apex  are  numerous  small  scales  and  hairs  filling  up  the  space 
about  it  and   probably  associated  with   the  prevention  of  drying  up  of  the  stem 


THF,    YOUNG    SPOROPHYTK  75 

apex,  which  is  doiibl)  protected  by  these  scales  and  its  complete  inclosuie  in  the 
young  leaf  bases.  It  is  possible  that  these  scales  secrete  some  mucilaginous  sub- 
stance, although  there  was  no  evidence  of  this  in  the  stained  sections. 

In  this  plant  the  internodes  were  quite  solid  and  there  was  no  trace  of  the  large 
lacuna-  which  were  described  for  the  younger  plant.  Whether  the  presence  of  the 
lacun;c  is  due  to  any  differences  in  the  environment  remains  to  be  seen.  The  speci- 
mens were  all  collected  under  apparently  the  same  conditions,  but  it  is  possible  that 
there  may  have  been  differences  in  the  amount  of  water  in  the  soil  in  which  they  were 
growing,  and  this  difference  in  the  amount  of  water  may  have  something  to  do  with 
the  development  of  the  lacunae. 

The  root  at  the  base  of  the  third  leaf  was  cut  transversely  and  was  in  a  ver)- 
early  stage  of  development.  The  root  was  still  completely  buried  in  the  cortex  and 
the  stele  still  imperfectly  developed,  but  showing  its  connection  with  the  stele  of 
the  fourth  leaf  above  the  junction  of  the  third  leaf  trace  with  the  stele  of  the  inter- 
node.  No  tracheary  tissue  was  developed  and  the  course  of  the  leaf  trace  was  bur 
little  disturbed  by  the  formation  of  the  root. 

In  longitudinal  sections  taken  from  a  much  older  sporophyte  (fig.  48,  C,  D) 
the  arrangement  of  the  organs  at  the  apex  is  seen  to  be  exactly  the  same  as  in  the 
younger  plants,  but  of  course  the  parts  were  all  larger.  The  youngest  leaf  (/ '  )  still 
resembles  in  form  and  size  the  corresponding  leaf  in  the  younger  stem,  but  the  next 
older  leaf  is  relativel)'  broader  than  the  early  leaves  of  the  younger  sporophyte,  and 
although  the  stipular  sheath  is  now  well  developed  the  upper  portion  of  the  leaf 
is  still  quite  undifferentiated  and  the  apex  is  scarcely  bent  forward  at  all.  The 
resemblance,  therefore,  to  the  young  leaf  of  Botrychinni  liiuario  is  even  more 
marked  than  it  is  in  the  younger  sporophyte.  The  apical  region  of  this  young  leaf 
is  occupied  by  an  epithelium-like  layer  of  columnar  cells,  and  it  is  doubtful  whether 
any  one  of  these  can  be  certainly  denominated  the  apical  cell.  Somewhat  the  same 
doubt  exists  also  as  to  the  point  of  a  single  initial  cell  in  the  youngest  leaf.  In  the 
latter  there  was  some  shrinkage  in  the  group  of  large  meristem  cells  at  the  apex, 
which  made  it  still  more  difficult  to  decide  this  point,  but  a  median  section  showed 
somewhat  indistinctly  a  single  cell,  apparently  triangular  in  outline,  which  from  its 
form  and  the  arrangement  of  the  adjacent  cells  may  very  well  have  been  the  apical 
cell.  The  small  group  of  meristem  cells  forming  the  stem  apex  is  crowded  in  between 
the  base  of  the  youngest  leaf  and  the  elongated  ridge  which  surrounds  the  stem  apex 
upon  the  ventral  side.  In  consequence  of  this  crowding  the  outer  faces  of  the 
apical  cell  and  its  youngest  segments  are  very  small.  The  base  of  the  apical  cell 
is  more  than  twice  as  broad  as  its  free  outer  face.  The  ventral  face  of  the  apical 
cell  is  convex  and  the  young  segments  cut  off  from  it  are  strongly  curved.  The  inner 
or  basal  wall  is  oblique,  so  that  the  axis  of  the  young  cells  in  the  tissue  below  the 
apical  cell  makes  an  angle  with  the  long  axis  of  the  apical  cell. 

Below  the  apical  region  may  be  seen  the  section  of  the  large  central  stele  of  the 
internode.  This  is  composed,  apparently,  of  two  strands  of  procambium  separated 
by  a  broad  band  of  pith.  As  Farmer  pointed  out,  in  the  older  plant  there  is  no 
question  that  procambium  tissue  is  developed  upon  the  ventral  side  of  the  bundle 
which  extends  into  the  apical  region  and  which  is,  apparently,  not  connected  with 
the  leaf  traces.     From  this  he  believes  that  the  stele  is  really  a  cauline  structure. 

A  study  of  the  cross-sections,  however,  as  will  be  presently  seen,  shows  that 
this  ventral  tissue  really  does  belong  to  the  leaf  traces,  although  it  is  possible  that 
the  basal  tissue  of  the  roots  may  :idd  to  it  in  parr,  bur  I  have  not  been  able  to 
satisfy  myself  that  any  of  this  stelar  tissue  can  be  |ii(i|nrl\  assigned  to  the  nctivit\- 
of  the  stem  apex. 


76 


THE    OPHIOGLOSSALES 


As  in  Botrychium  and  Ophioglossuni,  the  tissue  derived  immediately  from  the 
activity  of  the  apical  meristem,  after  the  central  pith  is  developed  in  the  stele, 
contributes  only  to  this  central  region  or  pith,  which  is  really  not  part  of  the  stele 
proper.  On  the  dorsal  side  of  the  stele  the  whole  of  the  procambial  strand  can 
easily  be  followed  into  the  leaf,  and  when  this  is  followed  downward  it  is  seen  to 
run  obliquely  through  the  youngest  internode,  at  the  base  of  which  it  joins  the  next 
leaf.  The  latter  already  has  its  lamina  developed  and  strongly  bent  over,  but  is 
still  inclosed  in  the  stipular  sheath  belonging  to  the  next  older  leaf. 

These  older  leaves  have  only  a  single  leaf  trace,  but  it  divides  into  two  strands 
above  the  level  of  the  stipular  sheath.     A  median  section  of  the  thick  central  stele  in 


F.r..5,. 


transverse  sect 

ions  from  a  young  sporophyt. 

:  of  Helrr. 

•  hthoMclr 

termi;i.nl  bud  i 

nclosed  by  stipular  sheath,  j/;. 

.    In  G,  V 

is  pit  bet^ 

[,  section  of  a  yc 

)ung  leaf,  showing  the  ternate  1 

amina. 

Xj;.     /,  petiole  of  leaf; 


the  upper  region  shows  conspicuous  protoxylem  elements  made  up  of  much  elongated 
tracheids,  whose  thickenings  are  between  annular  and  spiral  in  form,  but  very 
different  from  the  coarsely  reticulate  and  the  conspicuously  pitted  tracheids  of  the 
meta.xylem  developed  in  the  older  parts  of  the  stele.  In  all  cases  where  truly  median 
sections  were  seen  the  protoxylem  elements  occupied  the  innermost  region  of  the 
xylem  and  no  metaxylem  was  seen  within  these,  so  that  the  bundle  (at  first,  at  any 
rate)  is  endarch,  as  in  the  other  Ophioglossaceae.  It  is  impossible  to  see  in  this  sec- 
tion that  metaxylem  was  developed  inside  of  the  protoxylem,  as  Farmer  found  to  be 
the  case  in  the  older  sporophytes. 


THK   voi'Nc;  sroKoi'nii  i:  77 

In  fig.  48,  I\  iluic  is  sliowii  .111  insntiDii  oC  ;i  nnit  ii|i(in  ilic  side  .nul  its  vi-ry 
broadly  expaiuU-d  li;isc-  with  rlu-  iini;iil;n  rnn|umti\i  1 1  ailuuls.  I  Ins  \ii\  l)ici;i(l 
base  of  insertion  ami  ilu  dlnimis  c<mtimiit\  ol  tin-  ii.u  lu  ai\  tissiu-  ^A  tin  iciot  with 
that  of  the  central  stele  of  the  stem  siiggist  tiiat  tin  \rntial  jiait  of  the  stele  iiiiuht 
be  made  up,  in  pait  at  least,  of  toot  traces. 

Cross-sections  of  oldei  plants,  such  as  that  slioun  m  the  seiies  indieateil  in 
Hg.  51,  show  issentialh'  the  same  arrangement  di'  the  parts  as  d<i  the  Mummi  ones. 
.\t  the  ape.\  theie  ma\-  be  seen  in  section  the  three  \uungest  lea\es,  which  wc  will 
tlesignate  ies|iectively  1,  2,  and  i,.  No.  1  being  the  oldest  leaf  shown.  In  this  section 
the  oiliest  leaf  shows  two  vasculai  bundles  in  the  petiole,  and  this  is  tiiie  also  of  the 
secoml  leaf,  which  is  contained  within  the  stipiilar  sheath  of  the  oldest  leaf.  I'he 
lamina  of  leaf  No.  i  ainath  shows  the  characteristic  ternate  form.  I'he  \oung 
leaves  make  an  angle  of  ahoiif  ^o''  with  each  other.  Section  H  passes  directl\  thioiigji 
the  stem  a|)e.\  ami  shows  the  sections  of  the  basal  part  of  the  sheath  of  the  two  older 
leaves.  The  stipular  sheath  of  the  youngest  leaf  paitiall}'  incloses  the  stem  apex, 
and  surrounding  the  apical  tegion  is  a  loose  mass  of  cells,  derived  partly  from  the 
tissue  immediately  around  the  stem  apex  and  parth  from  the  edges  of  the  sheath 
of  the  youngest  leaves.  These  cells  are  realb  sections  of  hairs  and  scales  which 
perhaps  secrete  mucilaginous  matter,  but  there  was  no  evidence  of  this  in  the  sec- 
tions. Turned  towaitl  the  doisal  side  of  the  section  may  be  seen  the  leaf  tiace  fVom 
the  second  leaf  and  separated  fVotn  it  by  a  considerable  space  on  the  ventral  side 
is  a  rather  vagueb  deHmil  mass  of  young  procambium,  which  marks  the  trace  of 
the  youngest  leaf".  ( )n  the  ventral  side  of  the  latter  is  the  stem  apex  itself.  Further 
down,  as  has  already  been  described  for  the  younger  stem,  the  two  leaf  traces  apjiroach. 
At  the  level  of  the  stem  apex  the  trace  of  the  second  leaf  is  clearly  defined  and 
nearly  oval  in  outline,  but  more  convex  upon  the  dorsal  side.  I  he  bundle  is  inclined 
toward  the  side  of  the  stem  opposite  the  insertion  of  the  first  leaf.  Further  down 
the  trace  becomes  much  broader,  this  being  mainly  due  to  the  development  of  the 
tissue  upon  one  side,  which  begins  to  bend  downward  toward  the  ventral  side  of  the 
stem.  Fhe  trace  of  the  youngest  leaf  is  now  somewhat  better  defined  and  appears 
somewhat  kidney-shaped  in  section,  the  convexity,  like  that  of  the  second  leaf  trace, 
being  turned  toward  the  dorsal  side.  This  trace  also  begins  to  show  the  extension 
of  tissue  toward  the  ventral  side  of  the  stem  and  this  is  developed  on  the  side  opposite 
to  the  extension  in  the  next  older  leaf  trace.  Ultimately  these  ventral  extensions  of 
the  two  bundles  meet  as  the  two  leaf  traces  come  nearer  together,  and  the  dorsal 
ends  also  finally  come  into  contact,  so  that  the  two  bundles,  the  section  of  each  of 
which  is  approximately  semicircular,  form  a  complete  ring  inclosing  a  greater  or 
less  amount  of  the  ground  tissue,  which  thus  forms  the  pith  of  the  hollow  stele.  The 
stele  resulting  from  the  union  of  the  two  leaf  traces  is  not  at  first  perfecth-  circular 
in  section,  but  shows  plainly  for  a  long  time  that  it  is  composed  of  two  separate 
bundles  (fig.  51,  F). 

Fhe  first  development  of  permanent  tissue  in  the  older  leaf  trace  is  evident 
before  it  joins  the  younger  one.  The  first  elements  are  thick-w^alled  cells  (which 
may  be  called  protophloem)  in  the  outer  /one  of  the  phloem,  and  a  little  later  at  the 
inner  limit  of  the  bundle  a  small  group  of  protoxylem  elements  appears.  Very  soon 
after  this  a  similar  differentiation  takes  jilace  in  the  younger  leaf  trace,  so  that  when 
the  two  leaf  traces  are  completely  fused  the  protoxylems  have  the  appearance  of 
liaMns;  arisen  toward  the  central  part  of  tin  bundle,  but  in  reality  the  component 
bumlles,  at  least  at  their  earlier  stage  of  development,  may  be  described  as  endarch 
and  agree,  therefore,  with  the  bundles  of  the  other  Ophioglossacea*.  In  the  leaf 
traces  of  the  older  part  of  the  stem,  however,  theie  may  generally  be  found  inside 


78 


mOGLOSSALES 


the  protoxylem  a  few  scattered,  large  tracheary  elements,  so  that  the  bundle  may  be 
said  to  be  mesarch,  as  Farmer  states  is  the  case  in  the  older  rhizome. 

During  its  earlier  stages  the  stele  shows  no  leaf  gaps  where  the  leaf  traces 
depart,  and  the  leaf  gaps  are  only  gradually  developed.  Soon  after  the  stele  has 
assumed  the  form  of  a  hollow  cylinder  the  leaf  gaps  are  for  some  time  absent,  or 
they  are  developed  only  in  a  very  small  degree  and  close  almost  immediateh  upon 
the  departure  of  the  leaf  trace. 

In  none  of  the  young  plants  that  I  examined  could  I  detect  any  of  the  inner 
endodermis  which  occurs  in  the  older  rhizomes.  Farmer,  however,  states  that  the 
inner  endodermis  is  only  imperfectly  developed  and  concludes  that  it  is  the  result 
of  the  invagination  of  the  outer  endodermis  through  the  leaf  gap;  or,  to  put  it  in 
another  way,  it  is  the  persistence  of  the  inner  endodermis  of  the  leaf  traces  of  which 
the  hollow  stele  is  made  up.  The  bundle  at  this  stage  most  nearly  resembles  that  of 
Botryrhiuni  Iiiiuiritu  differing  from  that  of  B.  vtrgimaiunn  in  the  absence  of  a  true 


A.  Section  of  the 

B.  Stele  from  lov 

C.  Part  of  centra 


central  stele  of  Helnitnlhostachvs,  showing  the  two  xylems. 
t  of  an  older  sporophyte,  showing  junction  of  a  leaf  trace  with  t 
more  highly  magnified. 


cambium,  the  outer  wood  cells  being  directly  in  contact  with  the  inner  cells  of  the 
phloem.  Occasionally,  however,  there  may  be  seen  on  the  outer  edge  of  the  .xylem 
ring  a  few  imperfectly  developed  tracheids  which  probably  represent  a  very  rudi- 
mentary development  of  secondary  wood,  but  there  is  no  other  sign  of  the  definite 
cambium  zone  which  is  so  conspicuous  in  the  stele  oi Botrychium  virginianum. 

From  this  study  of  the  development  of  the  leaf  traces,  following  them  from  the 
stem  apex  downward,  it  appears  that  the  cylindrical  stele  in  Helminthostachys 
arises  in  precisely  the  same  way  as  that  of  Botrychium,  viz,  by  the  union  of  the  leaf 
traces.  The  appearance  of  procambium  upon  the  ventral  side  of  the  stele,  which 
in  longitudinal  section  appears  to  be  derived  directly  from  the  stem  apex,  can  thus 
be  explained  by  the  ventral  extension  of  the  broad  leaf  traces  which  meet  on  the 
lower  side  of  the  stem  as  well  as  above,  and  the  cylindrical  stele  is  thus  developed. 


79 


It  is  not  ini|)(issilil(  th.it  tlic  kmh  tiiuis  m.i\  also  cdntiihiitf  to  some  (.xtciit  to  the 
development  ot  this  \ intr;il  poi tioii  ot  tin-  stilt .  The  xyleni  masses  belonging  to  the 
two  leaf  trails  lemain  ijuite  ilistimt  tor  a  long  time,  the  one  belonging  to  the  older 
trace  being  better  develo|ied  than  that  trom  the  younger  one  (fig.  52,  A).  The 
metaxylem  consists  of  scattered  tracheids  arranged  regularly  in  an  arc  outside  the 
protoxylem  of  the  older  bundle,  but  there  are  a  few  scattered  smaller  ones  lying  in 
the  tissue  separating  the  two  primar\-  wiems.  so  that,  as  we  ha\e  seen,  the  bundle 
may  perhaps  be  described  as  mcsarch,  aiul  not  iiidanh  as  it  is  m  Ojilimoloisiini  and 
Botr\iliintii. 

The  two  wlenis  of  the  separate  bundles  are  tinalh  coniucted  b\  intermediate 
trachear)-  tissue,  so  that  a  iuarl\-  complete  ring  of  wood  is  formed;  but  the  xylem  of 
the  older  leaf  trace  is  still  clearly  recognizable  on  account  of  its  greater  thickness. 
In  the  section  figured  (rig.  52,  6")  there  is  no  tracheary  tissue  yet  formed  inside  the 
protoxylem  and  there  is  a  well-marked  pith  occupying  the  center  of  the  stele.  The 
endodermis  is  now  well  developed  and  inside  it  are  about  two  rows  of  pericycle  cells. 
The  protophloem  is  less  conspicuous  than  in  the  younger  stele  and  is  best  developed 
in  the  outer  portion  of  the  older  leaf  trace.     The  rest  of  the  phloem  is  made  up  of 


A.  Transverse  section  of  apex  of  first  root  of  Helminthostachys^  showing  a 

single  tetrahedral  apical  cell.    X200. 

B.  Apex  of  a  later  tetrarch  root,  with  apparently  no  single  initial  cell. 

thin-walled  cells,  the  larger  of  which  are  presumably  young  sieve  tubes.  The  section 
is  taken  from  a  much  older  part  of  the  stem  and  shows  that  the  bundle  has  attained 
practically  the  same  condition  as  in  the  adult  stem,  except  for  the  absence  of  the 
inner  endodermis.  The  central  pith  is  surrounded  by  an  unbroken  ring  of  wood, 
averaging  about  three  cells  in  width.  The  outer  part  of  the  bundle  is  essentially 
the  same  as  in  the  one  that  has  been  described. 

The  canal  described  by  Gwynne-Vaughn  for  the  older  sporophyte  is  plainly 
evident  here  and  extends  backward  from  the  sheath  cavity,  appearing  in  cross- 
section  as  a  narrow  cleft  between  the  inner  side  of  the  leafstalk  and  the  internode 
(rig.  49,  D,  v).  It  is  evidently  not  a  cavity  in  the  cortex,  but  merely  an  invagination 
of  the  epidermis,  which  is  continuous  with  that  of  the  inner  surface  of  the  stipular 
sheath. 

A  peculiar  feature  of  the  ground  tissue  in  the  young  stem  and  petiole  in  HcUnin- 
thostachys  is  the  pre.sence  of  cells  containing  roundish  bodies  which  stain  very 
strongly  with  Bismarck  brown,  and  these  cells  closely  resemble  the  tannin  cells  of 
the  Marattiace;e,  with  which  they  are  probabh'  homologous  (rig.  49,  6).  I-ang 
figures  these  cells  (Lang  I,  fig.  65),  but  makes  no  mention  of  them  in  his  text. 


80 


THE    OPHIOGLOSSALES 


The  trace  for  the  second  leaf,  the  first  functional  one,  is  usually  provided  with 
a  single  undivided  bundle  passing  through  the  petiole,  but  sometimes  this  divides 
into  two,  as  it  does  in  the  cotyledon  of  Botrychiiim  virgtiiuinum.  Where  a  single 
bundle  occurs  in  the  petiole  it  occupies  a  nearly  median  position  and  is  concentric 
in  structure,  although  the  phloem  is  somewhat  less  developed  upon  the  adaxial  side. 
The  xylem  consists  of  a  large  mass  of  tracheids  surrounded  by  the  phloem,  which  is 
reduced  to  about  two  rows  of  cells  upon  the  adaxial  side.  Whether  the  largest  cells 
in  this  portion  were  sieve  tubes  was  not  determined.  Where  two  bundles  are  present 
they  are  somewhat  smaller  and  are  more  nearly  circular  in  outline  than  the  single 
bundle,  which  they  resemble  in  structure.  In  the  ground  tissue  are  large  inter- 
cellular spaces  which  disappear  at  the  base  of  the  leaf,  where  the  ground  tissue  in 
cross-section  appears  almost  solid.  This  development  of  lacunas  in  the  first  foliage 
leaf  recalls  the  similar  ones  in  the  cotyledons  ui~  Botrychiutu  and  Opiiioglossiim. 

In  the  older  part  of  the  rhizome  there  is  a  slight  development  ot  periderm  on  the 
dorsal  side,  which  Farmer  found  to  be  the  case  also  in  the  older  rhr/,ome.  This 
periderm  is  restricted  to  the  dorsal  region  and  is  obviously  associated  with  tiie  leaf 
bases,  as  it  is  in  Botrvi/mun  and  probably  also  in  Opliioglosiiini.     It  presumably 


F,G.  54. 


Df  an  older  sforophyte  of  HelmimhosiMhys.   > 
sheath  is  absent  from  the  third  youngest  leaf. 


acts  as  an  absciss  layer,  such  as  Jeffrey  demonstrated  in  Botrycluum,  and  this  not 
only  causes  the  separation  of  the  old  leaves  but  perhaps  also  acts  as  a  protective 
layer  to  the  leaf  scars.  The  absence  of  periderm  from  the  ventral  side  is  no  doubt 
connected  with  the  strictly  dorsal  position  of  the  leaves. 

The  later  roots,  like  the  first  one,  grow  from  a  single  tetrahedral  apical  cell, 
very  much  like  that  of  Ophioglossum  and  Botrychiiim.  The  root  cap  is  not  very 
prominent  and  is  usually  somewhat  pointed.  It  apparently  owes  its  origin  entirely 
to  the  activity  of  the  outer  segments  of  the  apical  cell.  The  primary  segments  of 
the  root  cap  undergo  periclinal  divisions,  but,  as  in  Botrychiiim,  the  stratifications 
of  the  older  layers  is  much  less  marked  than  it  is  in  the  ordinary  ferns.  Each  of 
the  lateral  segments  of  the  apical  cell  divides  by  a  somewhat  radially  placed  anti- 
clinal, so  that  a  transverse  section  of  the  three  youngest  segments  shows  six  cells 
having  a  nearly  radial  arrangement.  Periclinal  walls  may  arise  and  the  inner  cells  of 
the  segments  give  rise  to  the  central  cylinder  of  the  root,  while  from  the  outer  ones 
is  developed  the  cortex.    As  in  the  other  Ophioglossaceae,  no  root  hairs  are  formed. 


Till':   ■souNc;  spoRonivri  (SI 

The  piiniaiy  root,  as  Lang  pointed  out,  is  usiiall)  tiiauli,  liiii  occasional!) 
iliarch  loots  occur,  as  they  usually  do  in  Botrychium  and  in  Ophioglossum  pciidii- 
linii.  In  this  case,  however,  one  of  the  xylems  was  rather  larger  than  the  other. 
The  later  loots  are  tetiarch  and  in  the  older  sporophyte.  as  Farmer  showed,  the 
roots  {feneially  lia\i  si\  wiem  masses,  or  occasionally  seven.  This  type  of  root  is 
most  like  that  of  the  Maiattiacex.  The  cndodermis  is  pretty  well  developed,  but 
not  so  conspicuous  as  it  is  in  Botrychium. 

In  the  cortical  region  of  the  first  root  there  is  a  /one  of  cells  in  which  occurs  an 
endophytic  mvcorrhiza,  such  as  is  common  in  the  roots  of  other  ( )phioglossacea-, 
and  probablv  the  same  as  the  endophytc  which  is  found  in  the  tissue  of  the  prothal- 
lium.  Whether  the  infection  of  the  primary  root  is  direct  from  the  prothallium  oi 
whether  there  is  a  new  infection  from  the  soil  was  not  determined.  Lang  states 
that  the  mycorrhiza  is  only  developed  in  the  first  two  or  three  roots,  the  fourth  root 
and  those  formed  later  not  having  the  endophytc.  In  these  later  roots  the  cortical 
cells  are  densely  filled  with  starch. 

The  rhizome  continues  to  grow  upright  for  a  good  while  and  it  was  not  deter- 
mined at  just  what  time  it  assumes  the  prostrate  position  which  it  has  in  the  adult 
form.  At  first  there  is  usually  one  root  formed  for  each  leaf,  but  in  the  older  plants 
this  regularity  is  lost,  and  Farmer  states  that  there  may  be  three  or  four  roots 
developed  for  a  single  leaf.  On  the  other  hand,  the  number  of  roots  may  be  less 
than  that  of  the  leaves,  especially  in  the  younger  plants. 

A  curious  abnormal  form  was  seen  in  a  young  sporophyte,  where  for  some  reason 
several  of  the  earliest  leaves  had  remained  in  the  rudimentary  condition  of  the  cotyle- 
don. Five  of  these  rudimentary  leaves  could  be  seen  formed  in  succession.  The 
sheaths  were  fully  developed  and  there  was  a  long  internode  between  each  pair  of 
leaves.  Three  of  these  had  developed  roots,  but  the  others  had  failed  to  do  so.  This 
rhizome  was  nearly  3  centimeters  in  length,  but  it  had  hardly  increased  at  all  in 
thickness.  A  single  ternate  leaf  had  expanded  at  the  summit,  but  whether  this 
was  the  first  functional  leaf  that  the  plant  had  developed  could  not  be  determined, 
as  the  rhizome  was  broken  off  below  and  there  may  have  been  one  or  more  func- 
tional leaves  developed  below  the  first  of  the  rudimentary  ones. 

This  repetition  of  vestigial  leaves  recalls  the  condition  of  things  in  Ophioglossum 
vulgatum  and  Botrychiiun  huuiria.  For  a  good  while  the  new  leaves  are  of  the  same 
ternate  form  as  that  of  the  first  foliage  leaf,  but  sooner  or  later,  probably  depending 
on  the  vigor  of  the  plant,  the  ternate  form  is  gradually  replaced  by  five  foliate  leaves, 
the  later  divisions  being  the  result  of  an  unequal  dichotomy  of  the  lateral  leaf  seg- 
ments, similar  to  that  by  which  the  second  lateral  segments  of  the  primary  leaf  are 
separated  from  the  terminal  leaflet.  In  these  five  foliate  leaves  the  characteristic 
"pecopterid"  venation  of  the  adult  sporophyte  is  fully  attained  (fig.  45,  B).  Kach 
lateral  vein  forks  twice,  the  ultimate  veinlets  extending  to  the  margin  of  the  leaflet. 
A  section  of  the  petiole  of  one  of  these  leaves  shows  that  it  contains  four  vascular 
bundles,  arranged  in  pairs.  The  dorsal  bundle  of  each  pair  is  decidedly  larger  than 
the  ventral  one.  The  base  of  the  petiole  is  almost  perfectly  cylindrical,  but  further 
up  it  becomes  winged,  so  that  a  groove  appears  on  its  inner  face  extending  for  some 
distance  below  the  junction  of  the  lamina  and  the  petiole.  1  here  is  a  very  slightl}' 
developed  hypodermal  tissue  composed  of  two  or  three  layers  of  cells,  the  walls  of 
which  are  colorless  and  considerably  thickened,  some  of  them  showing  thickened 
corners  like  the  collenchvma  found  in  the  leaves  of  the  Marattiacex. 


82  THE    OPHIOGLOSSALES 

COMPARISON  OF  THE  YOUNG   SPOROPHYTES  OF  THE  OPHIOGLOSSACE.E. 

If,  as  we  believe,  the  type  of  sporophyte  found  in  Ophioglossuni  moluccanum 
is  really  primitive,  we  may  assume  that  the  sporophyte  at  first  had  a  single  axial 
stele,  collateral  in  structure  and  essentially  the  same  in  leaf  and  root.  This  primitive 
sporophyte  had  no  stem  at  all,  but  consisted  simply  of  leaf  and  root.  From  the 
primitive  vascular  skeleton,  composed  of  a  single  unbranched  strand,  we  can  derive 
the  different  types  characteristic  of  the  older  sporophyte  in  the  three  genera.  As 
to  the  first  origin  of  the  stem  apex,  we  can  only  conjecture;  whether  it  originally 
arose,  as  it  does  in  Ophioglossum,  as  an  endogenous  structure  repeating,  as  it  were, 
the  origin  of  the  primary  root,  we  have  no  means  of  knowing,  but  this  seems  to  be 
the  most  probable  explanation  of  the  origin  of  the  stem  apex  in  the  primitive  sporo- 
phyte from  which  are  descended  the  different  types  of  the  Ophioglossaceae.  After 
the  establishment  of  the  stem  apex  the  secondary  leaves  contributed  their  quota  to 
the  developing  skeleton  of  the  sporophyte.  In  Ophioglossum  these  leaf  traces  remain 
largely  free  and  anastomose  only  to  a  limited  extent,  thus  giving  rise  to  the  open 
tubular  dictyostele  with  very  large  meshes.  The  structure  of  the  individual  strands 
of  the  dictyostele  is  essentially  the  same  as  that  of  the  free  leaf  traces. 

In  Helmmthostachys  the  early  leaf  traces  fuse  completely  and  there  is  formed 
a  solid  stele  in  the  younger  internodes  with  a  central  xylem  core,  composed  of  the 
united  xylems  of  the  two  leaf  traces.  These  leaf  traces  are  approximately  collateral 
in  structure,  although  it  may  be  that  they  have  a  small  amount  of  phloem  upon 
their  inner  face.  After  entering  the  petiole  of  the  young  leaf,  however,  these  assume 
a  distinctly  concentric  form.  As  the  leaves  increase  in  size  their  traces  become 
broader  and  in  section  appear  more  or  less  crescentic,  so  that  when  the  leaf  traces 
come  together  there  is  left  between  them  a  certain  amount  of  the  ground  tissue  which 
after  they  have  united  appears  as  a  pith  lying  inside  of  the  tubular  stele.  This 
pith,  however,  it  must  be  remembered,  is  not  part  of  the  stele  proper,  but  is  merely 
an  included  portion  of  the  ground  tissue.  With  the  complete  fusion  of  these  two 
broad  leaf  traces  the  tubular  form  is  established  and  the  wood  appears  in  section 
as  a  continuous  ring.  In  Botrychiitm,  especially  in  the  large  forms  like  B.  virgiti- 
tanitm,  the  tubular  condition  which  is  secondary  in  Helmmthostachys  is  established 
at  once;  this  is  probably  to  be  explained  by  the  fact  that  the  vascular  bundles  of 
the  first  leaves  are  much  better  developed,  there  being  two  strands  in  the  cotyledon 
and  in  the  second  leaf,  and  the  leaf  traces  belonging  to  these  are  correspondingly 
broad  and  on  fusing  include  at  once  a  certain  amount  of  the  ground  tissue,  so  that 
the  stele  appears  tubular  from  the  beginning.  Botrychium  virginuuiiim  undoubtedly 
represents  the  most  specialized  type  of  the  Ophioglossaceae,  and  the  development 
of  the  cambium  with  a  permanent  secondary  thickening  of  the  wood  is  an  evidence 
of  a  higher  degree  of  specialization  in  the  vascular  system  than  is  found  in  any  other 
living  Pteridophyte.  While  a  very  slight  indication  of  this  secondary  thickening 
has  been  found  in  Ophioglossum,  and  I  have  also  noted  some  slight  traces  of  it  in 
Helmmthostachys,  there  is  never  developed  in  these  the  genuine  cambium  ring,  such 
as  we  find  in  Botrychium  virginiarnim.  In  the  development  of  the  spiral  protoxylem 
elements  Helminthostachys  differs  from  the  other  Ophioglossaceae  and  suggests  the 
true  ferns.  In  the  early  development  of  its  vascular  system  there  rare  strong  sugges- 
tions of  some  of  the  Marattiacea?,  especially  Kaulfussia  and  Dancea.  The  develop- 
ment of  concentric  bundles  in  the  petiole  in  Helminthostachys  and  Botrychium 
also  suggests  the  Marattiaceae. 

Assuming  that  the  collateral  bundle,  which  is  typical  of  the  stem  in  all  of  the 
Ophioglossaceae  and  occurs  also  throughout  in  Ophioglossum,  is  primary,  the  con- 


THE    VOUNG    SFOROI'Il^l  !•:  83 

centric  bundles  as  they  occur  in  the  petiole  ot  Hcltnnithostacliys  and  liotrytliiutti 
must  be  considered  as  secondary.  Fhe  monarch  root  of  Ophioglossum  moluc- 
canum  and  the  other  members  of  the  section  Eiiophioglossum  is  to  be  considered 
as  a  relic  of  the  primary  condition  where  the  single  axial  stele,  as  in  the  young  spo- 
rophyte  of  O.  moluccanum,  had  the  single  strand  of  practically  uniform  structure, 
extending  through  the  leaf  and  root.  The  development  (jf  diarch  roots,  such  as 
those  of  O.  pt'iuliilinri  and  Botrvcliium,  is  probably  also  secondary  and  perhaps 
associated  with  the  early  development  of  the  second  leaf  in  these  forms.  The  diarch 
root  appears  again  in  the  young  sporophyte  of  the  Marattiaceae  and  is  permanent  in 
most  of  the  leptosporangiate  ferns.  The  roots  of  the  larger  species  of  Botryclutini 
and  especially  those  of  Helminfliostacliys,  with  their  increased  number  of  xylems, 
are  undoubtedly  secondary  developments,  perhaps  associated  with  the  large  size  of 
the  roots;  and  we  again  find  this  same  type  developing  in  the  Marattiaceae.  In 
regard  to  this  point,  Helminthostachys  is  the  most  aberrant  of  the  Ophioglossaceae 
and  approaches  nearest  to  the  Marattiaceae. 

The  leaf  in  the  smaller  species  of  Ophioglossum  is  probably  a  very  primitive 
structure  and  the  closed  stipular  sheath — which  is  not  exclusively  foliar  in  origin, 
but  at  first  owes  part  of  its  tissue  to  that  of  the  cortex  of  the  root,  from  which  the 
sporophyte  arises — is  probably  an  older  structure  than  the  strictly  foliar,  stipular 
sheaths  in  Botrychium  and  Helminthostachys.  The  simpler  types  of  Botrychium, 
like  B.  simplex  and  B.  hinaria,  show  a  transitional  condition  between  the  closed 
sheath  of  Ophioglossum  and  the  open  sheath  of  B.  virginiatnim,  which  may  really 
be  spoken  of  as  composed  of  two  stipules,  in  this  respect  recalling  the  Marattiaceae. 
Helminthostachys,  in  the  development  of  the  stipular  sheath,  agrees  exactly  with 
the  simpler  types  of  Botrychium.  In  these  forms  the  sheath  is  hood-shaped,  open- 
ing by  a  transverse  slit  in  front  and  below,  and  the  upper  portion  of  the  sheath  is 
broken  through  when  the  inclosed  leaf  emerges,  so  that  the  two  apparent  stipules 
in  Helminthostachys  are  really  secondary,  caused  by  a  tearing  of  this  hood-shaped 
sheath,  and  are  not  proper  stipules  as  they  are  in  Botrychium  virginianum. 

The  simpler  and  probably  more  primitive  species  of  Botrychium,  like  B. 
simplex  and  B.  luiiana,  are  obviously  intermediate  between  Ophioglossum  and 
the  larger  and  more  specialized  species  of  Botrvchiutri.  This  is  shown  in  the  form 
and  venation  of  the  leaves,  as  well  as  in  the  character  of  their  tissues.  Instead  of  the 
pinnate  venation  found  in  the  leaves  of  B.  virginianum,  these  more  primitive  species 
show  no  midrib  in  the  leaf,  but  the  veins  all  radiate  from  the  veins  of  the  leaflet, 
dividing  dichotomously,  so  that  they  are  arranged  in  a  fan-like  fashion.  Were  the 
iiuls  of  the  veins  connected  there  would  result  a  reticulate  venation,  exactly  like  that 
of  Ophioglossum.  These  leaves,  moreover,  are  fleshy  in  consistence  and  have 
stomata  upon  both  sides,  while  in  Botrychium  virginianum  and  in  Helminthostachys 
the  stomata  are  restricted  to  the  lower  surface  of  the  leaf  In  all  of  these  particulars 
Ophioglossum  and  the  simpler  species  of  Botrvcliium  are  evidenrh'  iimrc  primitive 
than  the  other  genera. 

In  Botrychium  virginianum,  as  we  have  seen,  the  c()t\ledon  is  extrauiilinarih 
developed,  more  so  than  that  of  any  other  Pteridophyte.  Ihe  contrast  between 
this  highly  developed  cotyledon  and  the  very  rudimentary  one  in  Botrychium  lunaria, 
where  the  yt)ung  sporophyte  passes  several  years  under  ground  before  the  first  green 
leaf  emerges,  is  very  striking.  It  is,  however,  to  be  assumed  that  the  rudimentar\ 
condition  of  the  leaves  in  Ophioglossum  vulgatum  and  Botrychium  lunaria  is  a 
secondary  condition,  connected  with  their  long  life  under  ground. 

Helminthostachys,  on  the  whole,  approaches  more  nearly  to  B.  lunaria  in  its 
early  stages  of  development  than  it  does  to  B.  viroinianum.      This  is  shown  in  the 


84  THE    OPHIOGLOSSALES 

rudimentary  condition  of  the  cotyledon  and  in  the  venation  of  the  first  foHage  leaf, 
which,  although  it  has  a  ternate  lamina,  is  quite  rudimentary.  We  have  already 
referred,  however,  to  the  rudimentary  leaves  of  B.  liiiiana,  which  also  sometimes 
develop  a  very  small  ternate  lamina.  The  venation  of  the  first  leaf  in  Hchnnithos- 
tachys  also  approaches  the  cyclopterid  type  found  in  the  leaves  oi  B.  hiiiana.  The 
structure  of  the  stele  in  the  young  stem  also,  after  attaining  the  tubular  form,  is 
more  like  that  of  5.  lunaria  than  like  that  of  5.  virgintanutti. 

On  comparing  the  early  stages  of  development  of  the  ( )phioglossace2'  and 
Marattiaceae  we  shall  find  that  they  have  a  good  many  points  in  common,  which 
will  be  discussed  more  at  length  after  we  have  described  the  structures  of  the  latter. 
Ophioglossiim,  as  to  the  formation  of  the  cotyledon,  is  very  much  like  Kaiilfiissia, 
while  Helmtnthostachys  is  more  suggestive  of  Dancca.  The  stipular  structures  of 
the  two  families  are  unquestionably  homologous  and  the  entire  conical  stipular 
sheath,  found  in  the  lower  members  of  the  Ophioglossace:e,  is  probably  an  older 
type  than  the  free  stipules  found  in  Botrychiiim  virginianum  and  the  Marattiaceae. 

In  both  the  Ophioglossaceae  and  Marattiaceae  the  young  sporophyte  at  first  is 
made  up  almost  entirely  of  leaf  and  root,  and  the  whole  vascular  system  is  composed 
of  the  leaf  traces  with  no  proper  cauline  vascular  tissues,  so  that  one  might  almost 
say  that  the  stem  is  made  up  entirely  of  the  bases  of  the  leaves,  the  dominance 
of  the  leaf  being  the  most  noteworthy  feature  in  the  morphology  of  these  plants. 
On  the  whole,  probably  Helminthostachys  most  nearly  resembles  the  Marattiaceae. 
This  is  true  both  of  the  character  of  the  venation  of  the  leaves,  the  structure  of  the 
root  bundles,  and  the  development  of  tannin  cells  in  the  young  sporophyte.  These 
tannin  cells  seem  to  be  quite  absent  from  the  tissues  of  both  OpJuoglossuni  and 
Botrychium. 


THE    ADULT    SPOROPHYTE  85 


IV.     THK  ADULT  SPOROl'inTI,. 

The  essential  characteristics  of  the  sporophyte  are  established  while  it  is  still 
quite  small  and  the  subsequent  differences  are  mainly  an  increase  in  the  size  of  the 
parts  and  finally  the  development  of  the  spore-bearing  structures  which  constitute 
the  peculiar  spike  or  sporangiophore  so  characteristic  of  these  plants.  As  the 
structure  of  the  tissues  has  been  repeatedly  studied  and  described,  no  attempt  will 
be  made  here  to  take  up  a  detailed  study  of  these. 

The  Ophioglossacea-  in  general,  except  for  the  rather  elaborate  vascular  bundles 
ot  the  stem,  especially  in  Botrychium,  are  marked  by  great  simplicity  in  the  structure 
of  the  tissues.  The  surface  is  usually  smooth  except  in  the  younger  plants,  where 
there  may  be  a  development  of  scales  and  hairs,  presumably  for  the  protection 
of  the  young  tissues  of  the  stem  apex.  The  hard  hypodermal  tissues  and  bands 
of  sclerenchyma,  so  common  in  the  leaves  and  stems  of  many  ferns  and  developed 
to  a  less  degree  in  the  Marattiacea?,  are  practically  entirely  absent  from  the  Ophio- 
glossacea;. 

Except  for  the  vascular  system  of  the  stem  the  bundles  are  usually  less  developed 
than  is  common  in  the  more  highly  differentiated  ferns,  this  being  especially  the  case 
in  Op/uuglossiini,  where  the  very  delicate  bundles  forming  the  veins  of  the  leaf  run 
through  the  spongy  green  tissue  of  the  leaf  without  causing  any  projecting  veins  at 
the  surface.  This  condition  is  true  also  in  the  simpler  types  o(  Botrychium  and  in 
the  young  leaves  of  Helminthostachys.  The  great  bulk  of  the  ground  tissue  in  leaf, 
root,  and  stem  is  parenchyma.  The  development  of  periderm  in  the  outer  tissues 
of  the  stem  is  probably  always  associated  with  the  leaf  bases  and  serves,  as  we  have 
seen,  both  to  separate  the  dead  leaf  bases  and  to  protect  the  scar  thus  left  after  the 
leaf  has  fallen  away. 

The  roots  are  characterized  by  the  complete  absence  of  root  hairs.  The  outer- 
most layer  of  cells  often  has  the  walls  much  thickened  and  they  mav  show  the  reac- 
tion of  cork.  The  bulk  of  the  cortex  of  the  root,  however,  is  composed  of  unmodified 
parenchyma.  The  vascular  cylinder  in  the  root  remains  monarch  in  the  section 
Eiwphioglossiim,  but  is  diarch  in  the  smaller  roots  oi  Ophioderma  and  in  the  smaller 
species  oi  Botrychium,  and  ranges  to  hexarch  in  the  larger  roots  oi  Helminthostach\s. 
The  roots,  especially  in  the  larger  species,  are  thick  and  fleshy  and  as  a  rule  branch 
sparingly  and  somewhat  irregularly.  In  the  section  Euophioglossum  no  lateral 
roots  are  formed  and  branching  is  rare.  When  it  does  take  place  it  is  the  result  of  a 
true  dichotomy  of  the  apex.  The  root,  as  in  the  youngest  stages  in  the  plant,  grows 
almost  always  from  a  single  tetrahedral  apical  cell,  which  is  much  alike  in  all  the 
genera. 

The  most  characteristic  feature  of  the  Ophioglossaceae  is  the  peculiar  sporangial 
spike  referred  to.  There  is  a  certain  correlation  in  the  degree  of  development  of  this 
spike  and  the  sterile  leaf  segment  with  which  it  is  associated.  The  fertile  leaves 
may  arise  very  early  in  the  history  of  the  sporophyte.  Bruchmann  states  that  the 
first  leaf  to  appear  above  ground  in  Botr\chium  lutuiria  is  already  a  fertile  one  and 
in  Ophioglossum  vulgatum  the  second  green  leaf  to  be  developed  usually  bears  spores. 
This  early  development  of  the  fertile  leaf  is  probably  an  indication  oi"  the  primitive 
nature  ot  these  plants,  as  we  must  assume  that  the  ancestral  form  must  have  at  once 
developed  a  sporangial  structure  on  the  first  leaf,  or  what  corresponded  to  that  in 
the  embryo.  In  liatrychium  luiuiria  Bruchmann  figures  )oimg  spore-bearing  plants 
which  are  still  connected  with  the  prothalliuni.  and  |effie\  states  that  in  B.ingiiii- 
anum  he  once  found  a  fruiting  plant  with  which  the  prothalliuni  was  still  connected. 


86 


THE    OPHIOGLOSSALES 


THE  SPOROPHYTE  OF  OPHIOGLOSSUM. 

Of  the  three  existing  genera  of  the  Ophioglossaceae,  the  genus  Ophioglossum 
is  much  the  largest  and  most  widespread.  The  number  of  species,  however,  is  very 
imperfectly  understood,  as  there  is  great  confusion  in  the  nomenclature,  owing  to 
the  inadequate  study  of  the  tropical  species,  of  which 
the  number  is  undoubtedly  much  greater  than  has 
generally  been  supposed.  The  smaller  terrestrial  species 
look  very  much  alike  and  it  is  evident  that  collectors  have 
often  failed  to  discriminate  among  them.  My  attention 
was  especially  called  to  this  while  I  was  collecting  ma- 
terial of  Ophioglossum  in  Java,  where  there  is  evidently 
a  considerable  number  of  species.  Raciborski  (Raci- 
borski  1),  who  has  described  the  Pteridophytes  of  this 
region,  mentions  only  a  single  species  as  occurring  in  the 
neighborhood  of  Buitenzorg,  where  most  of  my  collect- 
ing was  done.  But  in  that  immediate  neighborhood  1 
collected  at  least  three  very  distinct  species,  and  two 
were  collected  at  Tjibodas,  some  4,000  feet  above  Buit- 
enzorg. Raciborski,  however,  mentions  only  a  single 
species  as  occurring  at  Tjibodas.  There  is  no  doubt 
that  a  critical  study  of  these  plants  from  other  regions 
where  they  abound  will  greatly  increase  the  number  of 
species  to  be  recorded. 

The  great  majority  of  the  species  of  Ophioglossum 
belong  to  the  subgenus  Euophioglossum,  which  should 
probably  be  separated  completely  from  the  very  differ- 
ent forms  which  comprise  the  other  subgenera.  The 
species  of  Euophioglossum  are  all  small  or  moderate- 
sized  plants  with  undivided  leaves  which  are  generally 
lanceolate  or  broadly  oval  in  outline  and  have  the 
sporangial  spike  borne  on  a  very  long  stalk  attached  to 
the  sterile  part  of  the  leaf  near  the  base  of  the  lamina. 
These  plants  are  always  terrestrial,  the  leaves  growing 
from  an  upright  rhizome,  which  is  sometimes  a  good 
deal  enlarged,  sometimes  more  slender  in  form.  From 
the  rhizome  there  extend  numerous  roots  which  are 
sometimes  developed  one  for  each  leaf,  but  this  is  by 
no  means  always  the  case.  The  sporophyte  oi Euophio- 
glossum seldom  exceeds  a  height  of  30  to  40  centime- 
ters and  some  of  them  are  very  much  smaller  (fig.  55, 
also  plate  3). 

Except  for  their  larger  size  the  later  leaves  do  not 
differ  essentially  from  the  primary  leaf  of  the  young 
sporophyte.  The  venation  is  always  reticulate,  usually 
without  any  definite  midrib,  although  sometimes  there  is  a  central  vein  which  is 
slightly  stronger  than  the  others.  In  many  species,  e.  g.,  0.  moluccanum,  O.  vulga- 
tum,  small  branches  ending  blindly  are  found  within  the  large  meshes.  In  other 
species,  e.  g.,  O.  lusitanicum,  there  are  no  free  veins  within  the  areoles. 

In  many  of  the  species  but  one  leaf  is  formed  each  year,  but  in  others,  especially 
many   of  the   tropical  species,  there  may  be  as  many  as  four  or  five  formed  in  a 


F,G.55. 
Two  specimens  of  Ophioglossum  moluc- 
canum (Schlecht),  slightly  reduced. 
The  larger  one  is  the  typical  0. 
moluccanum ;  the  smaller  one  is 
probably  a  second  species. 


THE    Ain  I.T    Sl'OROl'UVTE  87 

single  season.  In  O.  vulgatum  the  development  ot  the  leaf  is  very  slow,  the  leaf 
remaining  three  years  inclosed  in  the  bud  and  emerging  in  the  fourth  season.  So 
far  as  I  know,  no  study  has  been  made  of  the  development  of  the  leaves  in  those 
species  of  the  temperate  climates  where  more  than  one  leaf  is  developed  in  the  season, 
and  it  remains  to  be  seen  whether  the  leaves  which  unfold  in  the  same  season  are 
of  the  same  age  or  not.  In  the  rapidly  growing  tropical  species  it  is  exceedingly 
unlikely  that  more  than  a  few  months  are  necessary  for  the  complete  development 
of  the  leaf,  which  unfolds  as  soon  as  it  is  mature,  but  nf)  data  are  available  on  this 
subject. 

While  the  spike  m  Euopliiogloisiirii  is  usuall)  inserted  at  the  base  of  the  sterile 
lamina  it  may  be  attached  much  further  down.  This  is  especially  noticeable  in  the 
small  species  O.  hcrgtanum,  from  South  America  (see  Bower  9,  page  435).  In  O. 
bergKinum  the  leaves  do  not  show  a  clear  separation  into  lamina  and  petiole  and  the 
spike  is  inserted  close  to  the  base  ot  the  linear  leaf,  so  that  it  appears  to  be  an  en- 
tirely distinct  structure. 

In  nearly  all  of  the  species  of  Euophioglossiim  the  later  roots,  like  the  primary 
ones,  are  monarch,  but  in  O.  bergunnim  they  are  diarch.  In  most  cases  at  least, 
as  Holle  (Holle  1)  showed,  only  one  root  is  formed  for  each  leaf.  This  seems  to  be 
the  case  in  O.  moluccanum,  which  was  investigated  with  some  care. 

Ophioglossum  pendulum  (plate  4,  B)  is  the  best-known  representative  oi  Ophio- 
derma,  the  second  section  of  the  genus.  This  differs  a  good  deal  in  its  general  char- 
acters from  the  small  terrestrial  species  of  Euophioglossum.  It  is  not  uncommon 
throughout  the  eastern  tropics,  where  it  grows  as  an  epiphyte  upon  the  trunks  and 
branches  of  various  trees.  The  rough  stems  of  certain  tree  ferns  and  some  palm- 
like species  of  Phcenix  form  a  favorite  habitat  for  this  fern  in  certain  regions  and, 
as  we  have  pointed  out  in  the  study  of  the  gametophyte,  it  is  frequently  found  rooting 
in  the  masses  of  humus  between  the  old  leaf  bases  of  some  epiphytic  ferns  like 
Asplentiim  nidus.  1  he  stem,  instead  of  being  upright,  is  markedly  dorsiventral, 
but  is  short,  with  the  leaves  crowded  together  near  the  end  and  all  growing  upon 
the  dorsal  side  of  the  rhizome,  as  they  do  in  Helminthostachys  (fig.  63).  The  leaves 
are  very  much  elongated  and  the  ribbon-like  lamina  merges  very  gradually  into  the 
extremely  stout  petiole.  These  leaves  in  large  specimens  may  reach  a  length  of 
1.5  meters,  or  even  more,  and  the  long,  strap-shaped  leaves  hanging  down  from  the 
boughs  of  the  trees  present  a  very  characteristic  appearance.  In  larger  specimens 
it  is  not  uncommon  to  find  the  lamina  dividing  dichotomously  (see  plate  4,  B)  and 
it  is  said  that  sometimes  this  dichotomy  may  extend  to  the  petiole,  in  which  case 
each  segment  of  the  leaf  bears  a  separate  spike. 

The  venation  of  the  leaf  is  reticulate,  the  veins  inclosing  long,  narrow  meshes 
with  no  free  veins,  and  the  venation  thus  resembles  the  type  represented  in  Euophio- 
glossum by  Ophioglossum  lusitantcum.  fhe  larger  plants  always  have  several 
leaves  which  are  expanded  at  the  same  time  and  growth  goes  on  uninterruptedly, 
The  leaves  are  crowded  together  and  there  is  no  evident  internode  between  them, 
but  it  is  clearly  seen  that  they  are  arranged  in  two  rows  on  the  fianks  of  the  short 
rhizome  (fig.  63,  A).  The  remains  of  the  stipular  sheaths  surround  the  bases  of 
the  leaves  and  these  sometimes  present  the  appearance  of  two  small  stipule-like 
organs.  As  in  Euophioglossum,  adventitious  buds  are  frequently  formed  upon  the 
roots.  As  a  rule  they  are  not  terminal,  but  lateral  structures  and  probably  do  not 
differ  essentially  in  their  development  from  those  of  O.  moluccanum. 

The  rhizome  is  more  or  less  buried  in  the  humus  and  the  roots  ramify  through 
this.  I^ven  in  the  very  young  plant  the  roots  are  branched  and  this  branching 
Ih-coiik-s  very  marked  in  the  larger  N]-)()roph\  fe.      There  seems  to  be  some  difference 


88  THE    OPHIOGLOSSALES 

in  the  number  of  roots,  but  in  most  cases  two  were  found  connected  with  each  leaf, 
instead  of  one  as  1  stated  in  my  earher  description  of  the  plant  (Campbell  4).  The 
roots  are  very  stout,  sometimes  attaining  a  diameter  of  over  3  millimeters.  The  smaller 
roots  are  diarch,  but  in  the  large  roots  there  may  be  three,  four,  or  even  five  xylems. 

Ophioglossum  poululiim  is  much  the  largest  member  of  the  Ophioglossaceae 
and  the  sporangial  spike  as  well  as  the  individual  sporangia  far  exceeds  in  size  those 
of  any  other  species  (plate  4,  B,  3-6).  The  spike  is  attached  by  a  short  peduncle  and 
hangs  down  from  the  pendent  lamina.  In  large  specimens  the  spike  may  reach  a 
length  of  20  centimeters  or  more  with  a  breadth  of  about  a  centimeter.  Above  the 
insertion  of  the  spike  the  leaf  is  thin,  but  the  slender  peduncle  is  continued  downward 
into  a  thick,  flattened  midrib  which  merges  gradually  into  the  petiole,  so  that  the 
spike  has  very  much  the  appearance  of  being  a  terminal  structure  with  the  sterile 
lamina  adherent  to  it. 

The  young  leaves  in  0.  pendulum  emerge  while  they  are  still  very  young  and 
the  sporangial  spike  is  in  an  extremely  rudimentary  condition  The  general  devel- 
opment of  the  leaf  is  therefore  very  easy  to  follow  in  this  species,  as  these  young 
leaves  are  entirely  free. 

The  second  species  of  the  section  Ophioderma  is  the  rare  O.  intermedium 
(fig.  69;  plate  4,  A).  This  for  a  long  time  was  known  only  from  one  locality  in 
Borneo,  but  has  lately  been  collected  at  other  points  in  the  Malayan  region.  The 
specimens  figured  were  collected  by  the  writer  near  Buitenzorg  in  Java.  In  the 
account  of  the  Ophioglossaceae  given  in  Engler  and  Prantl's  "Natiirliche  Pflanzen- 
familien"  (Bitter  2)  it  is  suggested  that  0.  intermedium  is  only  a  terrestrial  form 
of  O.  pendulum;  but  there  is  no  doubt  at  all  that  it  is  a  very  distinct  species.  The 
plants  described  here  were  growing  in  masses  of  humus  at  the  base  of  old  clumps  of 
bamboo.  The  stem  is  usually  very  short,  forming  a  small  tuberous  body,  from  which, 
in  most  cases,  only  a  single  leaf  was  growing,  although  two  were  sometimes  found. 
A  careful  examination  of  this  short  rhizome  showed  that,  like  Ophioglossum  pendu- 
lum, it  is  dorsiventral.  The  roots  were  short  and  in  all  cases  observed  were  without 
branches.  In  one  of  the  specimens  a  bud  very  similar  indeed  to  the  corresponding 
buds  in  0.  pendulum  was  found  growing  from  one  of  the  roots.  Ophioglossum 
intermedium  differs  from  O.  pendulum  in  being  rigidly  upright.  The  peduncle  is 
longer  and  the  lamina  of  the  leaf  much  smaller  and  more  clearly  differentiated  from 
the  petiole.  As  in  O.  pendulum,  however,  the  petiole  is  prolonged  into  the  peduncle 
of  the  spike  with  the  same  midrib-like  thickening,  caused  by  the  coherence  of  the 
basal  part  of  the  peduncle  with  the  lamina. 

This  plant  is  exceedingly  variable.  In  the  larger  specimens,  except  for  the  much 
shorter  lamina,  the  plant  a  good  deal  resembles  small  specimens  of  O.  pendulum. 
In  others,  however,  the  lamina  is  almost  completely  suppressed  and  this  condition 
closely  approaches  the  third  member  of  this  section,  Ophioglossum  simplex  (fig.  71). 
This  latter  species  is  at  present  known  only  from  one  locality  in  Sumatra,  and  is  dis- 
tinguished from  all  the  other  species  of  Ophioglossum  by  the  practically  complete 
suppression  of  the  sterile  portion  of  the  leaf  (see  Bower  8).  The  form  of  the  rhizome 
and  the  habit  of  the  plant  in  O.  simplex  most  nearly  resemble  0.  intermedium,  to 
which  it  is  probably  not  very  distantly  related.  Whether  or  not  we  regard  the 
absence  of  the  lamina  of  the  leaf  as  a  case  of  reduction,  the  fertile  leaf  in  0.  simplex 
certainly  very  closely  resembles  what  one  would  assume  to  have  been  the  primitive 
condition  of  the  leaf  in  the  ancestors  of  the  Ophioglossaceae. 

The  third  .section,  Cheiroglossa,  contains  a  single  very  peculiar  species,  O. 
palniatum  (plate  5).  This  occurs  throughout  tropical  America,  but  does  not  seem 
to  be  a  common  plant.     It  has  been  reported  from  Florida,  where,  however,  it  is 


THE    ADULT   SPOROPHYTE  89 

very  rare.  It  has  been  collected  in  various  parts  of  South  America  and  in  the  West 
Indies,  and  apparently  the  same  species  is  known  also  from  the  Island  of  Bourbon 
and  from  the  Seychelles  in  the  Indian  Ocean.  The  specimens  from  which  the 
figures  and  descriptions  given  here  were  made  were  collected  in  the  summer  of  1908 
in  the  Ulue  Mountains  of  Jamaica,  and  were  found  in  one  jihice  only,  growing  upon 
a  rotten  tree  stump. 

The  rhizome  in  Ophioglossitrn  palmatiim  is  an  almost  globular  tuber,  which  is 
radially  constructed  and  in  this  respect  resembles  that  of  Kuopluoglossum  more 
than  that  of  OphtoJcrma.  The  leaf  bases  are  covered  with  long  brown  hairs,  which 
give  a  characteristic  appearance  to  the  rhizome.  The  roots  are  numerous  and  more 
slender  than  those  of  Ophioglossum  pendulum.  They  are  sparingly  branched  and 
the  branching  may  have  the  appearance  of  a  true  dichotomy,  but  the  material 
available  did  not  allow  of  a  critical  investigation  of  this  point.  However,  since 
in  Euophtoglossum  the  branching  of  the  roots  is  actually  dichotomous,  it  is  not 
impossible  that  the  same  may  be  true  in  Cheiroglossa.  The  smaller  roots,  as  in 
O.  prnduhim,  are  diarch  and,  as  in  all  of  the  other  forms,  a  niycorrhiza  is  developed 
in  the  cortical  region. 

In  sections  of  one  of  the  largest  roots  available  the  bundle  was  triarch.  1  his 
root  was  rather  young  and  the  trachcary  tissue  was  only  partially  lignified.  The 
niycorrhiza  was  also  less  evident  than  in  the  smaller  roots  taken  from  a  younger 
plant.  Two  young  plants  were  found  which  probably  had  arisen  from  buds  upon 
the  roots  of  the  older  sporophyte.  One  of  these  is  shown  in  figure  70,  A.  It  had 
developed  a  single  nearly  lanceolate  leaf  very  much  like  the  early  leaves  of  O. 
pe)idulum.  A  single  root  had  developed  near  the  base  of  the  leaf  and  this  was  joined 
to  the  small  globular  rhizome.  A  second  root  could  be  seen  above  this,  but  whether 
this  second  root  belonged  to  the  leaf  or  was  part  of  the  root  upon  which  the  bud  had 
arisen  could  not  be  determined. 

The  older  leaves  may  reach  a  length  t)t  60  centimeters  or  more  (plate  5).  "1  hey 
are  more  or  less  deeply  palmately  cleft  into  narrow  segments,  which  give  the  leaf  a 
curious  superficial  resemblance  to  certain  kelps,  such  as  Laminana  digitata.  \  he 
base  of  the  fan-shaped  lamina  is  abruptly  narrowed  into  a  nearly  cylindrical  petiole, 
about  ecjual  in  length  to  the  lamina  itself.  The  venation  is  rather  of  the  type  of 
().  viilgdt  11)11,  having  numbers  of  free  veins  in  addition  to  the  elongated  closed  meshes. 

In  .some  of  the  smaller  leaves  (plate  5,  3)  there  is  present  a  single  small  median 
spike,  which,  like  that  of  O.  prnduhim,  has  a  short  peduncle,  but  it  is  inserted  below 
the  lamina,  in  this  respect  again  being  more  like  Euophioglossutn.  In  the  larger  leaves 
there  are  several  sporangial  spikes  arranged  in  a  series  on  either  side  of  the  petiole, 
usually  below  the  insertion  of  the  lamina,  but  sometimes  some  of  them  are  inserted 
above  the  junction  of  the  lamina  and  the  petiole.  Bower  (Bower  9,  page  436)  has 
figured  a  series  of  specimens  of  this  species  showing  the  great  variation  in  the  number 
and  arrangement  of  the  spikes.  He  emphasizes  the  fact  that  although  these  spikes 
are  apparently  marginal,  in  reality  they  always  ari.se  from  the  adaxial  side  of  the 
leaf.  1  ie  shows  that  in  this  species  also  there  mav  be  a  branching  of  the  individual 
spikes  sinn'lar  to  that  which  occurs  in  Opliioglnssum  prnduhim  and  less  frecjuently 
ill  ccirain   species  of   Kuopluoglossum. 

IHK  ANATOMY  OF   K UOPHIOGI.OSSIIM 

The  stem  aj^ex  of  the  adult  plant  has  been  repeatedK  studied  in  the  witlespiead 
Opluoalussunt  vulg/itum,  hut  thetc  is  little  information  in  regard  to  this  jioint  in 
other  species.  From  a  somewhat  careful  txamination  of  ().  mohutunum  it  is  eviilent 
that  this  species  agrees  dosel}'  with  ().  vulgntum,  and  a  study  by  one  of  mj-  students, 


90 


THE    OPHIOGLOSSALES 


Mr.  C.  S.  Morris,  of  this  species  and  also  ot  a  broad-leaved  form  from  Ceylon, 
probably  0.  reticulatum,  showed  that  the  same  characters  prevail  in  the  species  he 
examined  as  in  0.  vulgatum.  It  therefore  seems  likely  that  all  species  of  Euophio- 
glossum  agree  in  the  main  in  the  structure  of  the  stem  apex  and  the  development 
of  their  tissues. 

We  have  seen  that  in  the  young  sporophyte  the  stem  apex  is  completely  inclosed 
in  a  small  cavity  formed  by  the  hood-like  stipular  sheath  of  the  youngest  leaf.  This 
condition,  once  established,  is  permanent  (fig.  56)  and  there  is  no  essential  difference 
in  the  appearance  of  the  stem  apex  between  a  young  plant  in  which  two  or  three 


1  older  sporophyte  of  0 phioglosium  moluccanum,  showing  arrangement  of 
n  apex;  sp,  young  sporophylls.    D  shows  apical  region  more  enlarged. 


leaves  have  been  developed  and  the  full-grown  sporophyte.  The  stem  apex  is  of 
limited  extent,  crowded  in  between  the  bases  of  the  young  leaves,  and  in  O.  moluc- 
canum the  single  apical  cell  is  of  the  same  form  as  that  which  was  found  in  the  early 
condition  of  the  young  bud;  i.  e.,  in  longitudinal  section  it  is  four-sided,  with  a 
broad  base  and  a  narrower  outer  face.  According  to  Holle  (Holle  1),  the  apical 
cell  in  0.  vulgatum  is  pointed  below;  but  Rostowzew  (Rostowzew  2)  in  his  figures 
shows  the  same  form  as  the  apical  cell  in  O.  moluccanum.  It  is  not  at  all  impossible, 
however,  that  both  forms  may  occur,  as  in  cross-sections  the  apical  cell  in  O.  mol- 
//rr///;//^«  may  be  either  three-sided  or  four-sided  (figs.  ^Q   and    56,  D).     The  apical 


THE    ADULT   SPOROPHYTE 


91 


cell  in  O.  molurcanurti  may  rherefore  be  described  as  a  three-sided  or  four-sided  prism 
or  a  truncate  pyramid. 

As  in  the  young  plant,  the  sripular  sheath  of  each  new  leaf  is  formed  mainly 
from  the  basal  tissue  of  the  leaf  itself,  but  includes  also  tissue  from  the  margin  of 
the  stem  apex.  The  sheath  is  open  above  by  a  narrow  pore  through  which  it 
communicates  with  the  space  between  it  and  the  next  stipular  sheath.  In  O. 
moluccaniitn,  as  in  ().  vulgatiim,  three  leaves  of  different  ages  can  generally  be  seen 
inclosed  in  the  bud  and  sometimes  the  first  indication  of  the  fourth  young  leaf  can 


Six  of  a  scries  of  cross-sections  from  a  sporophyte  of  Ophio^lossum  molurcanum,    j/>,  young  sporophy!!;  x,  stem  apex. 

also  be  distinguished  (fig.  56,  C,D).  A  cross-section  of  the  youngest  sheath  shows 
the  pore  as  a  minute  opening,  separated  from  the  stem  apex  below  by  a  very- 
narrow  space. 

A  careful  study  of  the  older  stem  gives  no  reason  for  assuming  that  the  tissues 
of  the  very  open  reticulum  forming  the  fibrovascular  system  of  the  rhizome  is  in  any 
part  due  to  additions  from  the  apical  tissue  of  the  stem.  Whether  longitudinal 
or  transverse  sections  are  examined  it  is  perfectly  clear  that  the  strands  of  this 
reticulum  are  made  up  entirely  of  leaf  traces  which  can  be  readily  followed  into  the 
young  leaves  or  the  tissue  immediately  below.  The  immediate  apical  region  of  the 
stem,  as  in  the  younger  sporophyte,  is  unmodified  parenchyma  which  adds  onh'  to 
the  large  central  pith,  if  pith  this  can  be  called,  as  the  separate  bundles  of  which  the 
vascular  reticulum  is  composed  run  free  for  long  distances  through  the  ground  tissue 


92 


THE    OPHIOGLOSSALES 


of  the  Stem,  which  is  identical  in  appearance  in  the  cortical  and  the  central  regions. 
The  bundle  from  each  young  leaf  can  be  traced  to  a  junction  with  a  root  stele  and 
from  this  point  of  junction  it  extends  through  the  ground  tissue  of  the  stem,  running 
almost  horizontally  until  it  joins  the  trace  from  the  next  older  leaf.  In  this  way  is 
built  up  the  open,  large-meshed  vascular  cylinder.  So  far  as  could  be  determined 
in  O.  moliiccaiiiitii  only  one  root  was  formed  for  each  leaf.  The  tissues  of  the  root 
base  are  continued  upward  to  connect  with  the  young  leaf  and  downward  to  join  the 
stele  from  an  older  one. 

No  endodermis  can  be  detected  in  the  bundles  of  the  stem  in  O.  vulgatuni  and 
the  same  is  true  for  0.  moliiccamtm,  but  in  O.  bcrgianum,  0.  capense,  and  0.  ellip- 
iictim,  according  to  Poirault  (Poirault  2),  both  an  inner  and  outer  endodermis  occur 
in  the  older  part  of  the  rhizome;  these  however,  disappear  in  the  younger  region 
higher  up. 

A  transverse  section  of  the  mature  rhi- 
zome (fig.  57)  in  Ophioglossum  moluccanum 
shows  the  widely  separated  sections  of  the 
strands  of  the  vascular  cylinder  as  a  circle 
of  small  collateral  bundles  without  any 
endodermis,  the  mass  of  wood  being  in 
immediate  contact  with  the  thin-walled 
parenchyma  of  the  ground  tissue  or  sepa- 
rated from  it  at  most  by  a  single  row  of 
pericycle  cells.  In  some  of  the  smaller 
species  the  leaf  traces  are  relatively  broader 
and  there  is  an  approximation  to  the  ring- 
shaped  section  presented  by  the  cylindrical 
stele  of  Botrychium  or  Helminthostachys, 
and  sometimes  the  same  appearance  may  be 
approached  in  sections  of  the  older  rhizome 
which  happen  to  pass  through  a  region 
where  there  are  numerous  anastomoses  of 
the  bundles  forming  the  reticulum  (fig.  57,  E). 

Kxcept  for  the  vascular  bundles,  the 
tissue  of  the  stem  is  made  up  almost  ex- 
clusively of  simple  parenchyma.  The  de- 
velopment of  periderm,  which  takes  place 
to  a  limited  extent  in  the  outer  region,  is 
doubtless  associated  with  the  old  leaf  bases, 
as  it  is  in  Botr\chium. 

The  leaf  structure  of  £i/o/j/z/o^/oj-x//m  is 
exceedingly  simple.  The  mesophyll  is  made 
up  of  thin-walled  green  cells,  practically  uni- 
form throughout;  and  through  this  spongy  mass  of  mesophyll  the  delicate  veins  pass 
without  forming  any  projections  at  the  surface.  Both  sides  of  the  leaf  are  provided 
with  a  simple  epidermis,  stomata  being  developed  on  both  sides  of  the  leaf.  In 
those  species  in  which  the  leaf  lies  more  or  less  horizontally,  as  it  does,  for  example, 
in  O.  reticulatum ,  the  stomata  are  less  numerous  upon  the  upper  surface. 

The  arrangement  of  the  bundles  in  the  petiole  has  been  already  studied  in  the 
commoner  European  species,  O.  vulgatuni  and  O.  lusitmitcum.  In  all  of  the  species 
belonging  to  the  section  Euophioglossum  there  is  given  off  from  the  vascular  system 
of  the  rhizome  a  single  leaf  trace,  which  divides  at  the  ba.se  of  the  leaf  into  two 


section  of  a   sporophyte    of   Opiiioglo 
p;,  older  than  the  one  shown  in  fig.  56.   \  j 


■;r<)Rorm 


93 


stiaiuls.     I'.ach  of  tlusr  stiaiuls  ma\-  ilividi-,  oi  onl\  <.iu-  ol  tlKin  ( ti<i.  ho).     In  soim- 
of  the  smaller  species  there  are  only  three  hiindles  in  the  petiole,  and  in  these  foinis 

hase.     In  the  larger  species  these 

ction  is  greater.     Ihus, 

each  of  the  two  ventral  bundles  may  divide  again  in  tin  iipjier  region  of  the  petiole 
that  a  cros.s-section  at  this  point  would  show  h\i  hinulles,  a  large  dorsal  one 
id  two  pairs  of  sinallei  ventral  ones.     A  similar  condition  ol  things  is  touiul  in  tin 


there  are  no  anastomoses  of  the  bundles  above  the  ..«,i<.. 
branches  divide  further  and  the  number  of  bundles  in  tin 


Vascular  bundle  from  an  adult  rhizome  of  Opkiogloaum  moluccanum.     X 
Section  of  an  adult  root  showing  monarch  vascular  cylinder.     X35.    The 
is  occupied  by  the  mvcorrhiza. 


small  species.  0.  californiciim.  As  sections  are  examined  below  the  junction  of  the 
lamina  and  the  petiole,  it  can  be  seen  that  further  forking  of  the  bundles  has  taken 
place  preliminary  to  their  entering  the  lamina  itself.  Some  of  the  species  have  the 
tissues  of  the  petiole  quite  compact,  others  show  a  greater  or  less  development  of 
lacunae  or  air-spaces  in  the  petiole. 


[HE  ROOT  IN  EUOPHIOGLOSSUM. 


The  early  roots  in  O.  moluccanum  grow  from  a  large  tetiahedral  apical  cell 
showing  a  fairly  regular  segmentation,  much  like  that  of  the  typical  ferns;  but  the 
root  cap  is  not  so  well  developed  nor  does  it  show  as  definite  a  stratification.    In  the 


early  roots  the  whole  of  the  root  cap  seems  to  be  derived  from  the  outer  segments 
of  the  apical  cell.  In  the  later  and  larger  roots  there  seems  to  be  somewhat  less 
regularity  in  the  segmentation  and  no  sections  were  found  which  showed  the  apical 


94 


THE    OPHIOGLOSSALES 


cell  and  its  segmentation  as  clearly  as  in  the  younger  roots;  however,  only  a  small 
number  of  these  later  roots  were  sectioned  and  it  may  be  that  they  were  not  all 
quite  normal. 

A  section  of  an  adult  root  is  shown  in  fig.  59,5.  The  cortical  region  is  made  up 
of  simple  parenchyma  and  the  mycorrhizal  zone  is  very  conspicuous.  The  endo- 
dermis  is  not  very  clearly  defined,  less  so  than  in  the  earlier  roots,  and  its  limits  are 


Five  sections  of  a  full-grown  sporophyll  of  Qphiogloisum  molucranum.    E,  section  of  peduncle  of  spike;  /, 


not  easily  determined.  The  cortical  cells  inside  the  mycorrhizal  zone  are  densely 
filled  with  starch.  More  than  half  of  the  section  of  the  bundle  is  occupied  by  the 
large  solid  mass  of  wood.  This  is  separated  from  the  endodermis  by  a  single  layer 
of  pericycle  cells.  The  single  mass  of  phloem  lying  next  the  wood  is  not  much  more 
than  half  as  large. 

ANATOMY  OF  OPHIODERMA. 

Owing  to  the  dorsiventral  position  of  the  rhizome  and  to  the  more  rapid  de- 
velopment of  the  leaves,  the  section  of  the  stem  apex  in  Ophioglossiim  pendulum 
differs  a  good  deal  from  a  similar  section  oi  Euophtoglossitm  (fig.  64).  The  base  of 
the  leaf  is  bent  sharply  upward,  this  being  the  case  also  in  the  very  young  leaf  which 
is  inclosed  within  the  bud.  The  leaves  break  through 
the  inclosing  sheath  in  a  very  rudimentary  condition, 
although  of  such  size  that  a  section  through  the  base 
of  the  youngest  visible  leaf  shows  usually  but  a  single 
younger  leaf  inside  the  sheath,  instead  of  the  three  or 
four  that  are  seen  in  a  similar  section  of  the  bud  in 
EuQphioglossum.  Within  the  sheath  at  the  base  of  the 
youngest  visible  leaf  there  is  found  a  cavity  in  which  is 
the  growing  point  of  the  stem  and  the  youngest  leaf 
The  apex  of  the  stem  forms  a  strongly  inclined,  nearly 
plane  surface  and,  as  in  Euophioglossum,  the  growth  is 
from  a  single  apical  cell  which,  so  far  as  could  be  deter- 
mined, has  the  form  of  a  three-sided  pyramid,  whose 
lateral  faces  are  more  or  less  strongly  convex  and  whose  apex  may  be  truncate. 
F"rom  the  few  cases  observed  it  is  not  possible  to  say  definitely  whether  basal  seg- 
ments are  regularly  cut  off  as  well  as  the  lateral  ones.  The  segments  cut  off  from 
the  lateral  faces  are  large  and  the  divisions  irregular. 

Owing  to  the  large  size  of  the  sporophyte  there  are  practical  difficulties  con- 
nected with  the  study  of  the  vascular  system  of  the  rhizome  from  a  series  of  micro- 
tome sections.     The  numerous  bundles  in  the  leaf  base  do  not  unite  into  a  single 


E  root  of  0 phioglossuti 
1,  showing  dichotomy. 


a'OROI'HYTK 


95 


leaf  trace,  but  pass  downward  througli  the  cortex  separately,  and  even  it  it  were 
possible  to  make  a  satisfactory  series  of  the  sections  of  the  large  rhizome  the  task  of 
following  the  course  of  the  very  numerous  individual  bundles  would  be  a  difficult 
one.  From  free-hand  sections  of  the  large  base  of  the  leaf,  however,  one  can  see 
without  difficulty  the  general  plan  of  the  vascular  skeleton.  The  stout  petiole  is 
slightly  contracted  at  its  base,  but  a  section  presents  very  much  the  same  appear- 
ance as  one  made  higher  up. 

In  specimens  that  have  been  preserved  in  alcohol  so  as  to  become  decolored, 
the  tissues  of  the  thick  leaf  base  are  sufficiently  transparent  to  show  quite  clearly 
the  course  of  the  bundles  even  without  sectioning,  by  simply  slitting  the  petiole 
through  the  middle.  The  bundles  are  seen  to  anastomose  freely  at  the  extreme  base 
of  the  leaf,  very  much  as  thev  do  in  the  lamina.  If  such  a  section  is  examined  where 
the  leaf  base  joins  the  rhizome  (fig.  63,  ]))  the  circle  of  bundles  can  be  seen  to  become 


A.  Stem  showing  dorsivcntral  form  and  branched  roots.    /,  bases  of  leaves. 

B.  Buds  attached  to  a  root  fragment.    The  older  bud,  6',  has  developed  a  younj*  sporophyll,  j/j,  and  two  sec<)nJary  roots. 

C.  Base  of  a  large  leaf,  showing  arrangement  of  vascular  bundles. 

D.  Section  of  same. 

smaller  as  the  bundles  enter  the  cortex,  but  the  bundles  remain  for  the  most  part 
quite  separate,  although  there  may  be  an  occasional  anastomosing  of  these,  as  occurs 
in  the  petiole  itself.  This  group  of  bundles  composing  the  leaf  trace — if  such  it 
can  be  called — forms  a  circle  about  the  opening  in  the  vascular  cylinder  of  the  stem 
where  it  joins  the  latter.  A  section  of  the  vascular  cylinder  within  the  rhizome  itself 
presents  the  appearance  of  a  nearly  complete  ring,  which  is  probably  formed  by  fu.s- 
ing  of  the  bundles  derived  from  the  leaf  bases.  The  much  greater  development  of 
woody  tissue  in  the  stem  of  O.  pendulum  as  compared  with  that  of  Euop/iioglossutri 
is  doubtless  due  to  the  very  much  larger  size  of  the  leaves  and  the  correspondingly 
greater  number  of  vascular  bundles  contributed  by  them  to  the  woody  cylinder  of 
the  rhizome. 

The  very  young  leaf,  such  as  is  shown  in  fig.  63,  B,  has  a  thick,  fleshy  leaf  base, 
terminating  in  a  very  small  and  pointed  lamina  strongly  bent  over  as  it  is,  c.  g., 
in  the  young  leaf  of  Bolrvrhium  virgiriinnum.  This  differs  from  the  species  of 
Euopluoglossitm,  in  which  the  leaf  is  straight  in  the  bud.  llnder  the  arching  hood 
formed  by  this  folded-over  lamina  is  the  young  spike,  almost  equal  in  length  at  this 
time  to  the  lamina  itself.  A  somewhat  older  stage  is  shown  in  fig.  82,  B.  The 
leaf  has  now  become  somewhat  flattened,  but  as  yet  there  is  no  sharp  distinction 
between  the  lamina  and  the  petiole.  In  this  early  stage  of  development  the  inter- 
pretation of  the  spike  as  a  terminal  structure  seems  very  plausible.    An  interesting 


96  THE    OPHIOGLOSSALES 

case  is  shown  in  fig.  8z,  E,  where  the  lamina  is  almost  entirely  siippiesscd  and  the 
terminal  character  of  the  spike  is  very  evident. 

As  the  leaf  develops,  there  is  a  very  great  increase  in  size  in  the  lamina,  which, 
as  we  have  seen,  may  reach  a  great  length.     The  anatomical  structure  of  the  leaf 


A.  Section  of  stem  apex.     X3. 

B.  Young  sporophyll.    sp,  sporangiopho 

C.  Stem  apex,  x,  and  youngest  leaf,  /. 


-Ophioglossum  pendulum. 

D.  Tlie  stem  apex,  more  enlarged. 

E.  Very  young  sporophyll.     sp,  sporangiopho 


closely  resembles  that  of  Eiiophioglosstim,  but  the  stomata  are  much  larger  and 
around  the  stoma  is  a  concentrically  arranged  series  of  cells,  indicating  that  probably 
the  formation  of  the  mother  cell  of  the  stoma  is  preceded  by  a  series  of  preliminary 


Fig.  66. 

.A.  Section  of  petiole  of  a  sporophyll  of  ().  pnidului 

B.  Section  near  base  of  lamina,    sp,  base  of  spike. 

C-E.  Sections  of  peduncle  of  spike.    C  and  D  arc 

same  leaf;  E  from  a  laiger  one. 


divisions  in  the  epidermal  cell.  The  tissues  in  the  petiole  are  very  like  those  in  the 
lamina  of  the  leaf  except  that  they  are  somewhat  more  compact.  The  walls  of  the 
ground  tissue  in  this  region  are  very  deeply  pitted. 

The  structure  of  the  vascular  bundle  of  the  petiole  (fig.  65),  is  much  like  that  in 
Euophioglossum,  except  that  there  is  a  rather  greater  development  of  tissue  upon  the 


THK    ADULT    SPOROPHYTE 


97 


inin-r  side  of  tlie  wood,  so  that  there  is  a  slight  suggestion,  at  least,  ot  a  concentric- 
structure  of  the  bundle,  such  as  is  found  in  the  petioles  of  Botrychium.  The  xylem  is 
composed  entirely  of  tracheids  with  reticulate  markings.  The  rest  of  the  bundle  is 
made  up  of  sieve  tubes,  mingled  irregularly  with  smaller,  thin-walled  elements.  It 
,      \  could  not  be  certainly  deter- 

mined whetherany  sieve  tubes 
were  developed  on  the  inner 
side  of  the  wood. 

The  number  of  bundles  in 
the  petiole,  especially  in  large 
specimens,  is  much  greater 
than  in  any  of  the  species  of 
Euophioglossum.  In  a  spe- 
cimen of  medium  size  (fig.  66) 
eighteen  bundles  could  be 
seen,  of  which  probably  seven 
or  eight  are  destined  to  sup- 
ply the  spike.  In  the  fertile 
leaves  these  form  a  complete 
circle,  but  in  sterile  leaves 
there  are  no  bundles  on  the 
adaxial  side  of  the  section.  In  the  free  portion  of  the  peduncle,  which  is  relatively 
slender,  the  number  of  bundles  is  much  less  than  in  the  broad  basal  portion.  In 
the  smaller  specimen  figured  there  were  but  three  bundles  in  the  middle  part  of  the 
peduncle.  The  complete  absence  of  the  adaxial  strands  in  the  petiole  of  the  sterile 
leaf,  even  at  its  base,  is  a  strong  confirmation  of  the  view  suggested  by  both  the  older 
leaf  and  the  younger  stages,  that  the  peduncle  is  really  an  independent  structure 
whose  bundles  are  joined  directly  to  the  rhizome. 


Fic.  67. 
1  of  the  root  apex  of  Ophioglo: 


;  niycorrliiial  : 


O.  intertnciUum  (fig.  69)  closely  resembles  O.  petidulum  in  its  anatomy,  like  the 
latter  developing  stomata  upon  both  sides  of  the  leaf,  and  these  stomata  are  very 
large  and  show  accessory  cells  similar  to  those  found  about  the  stomata  of  O. 
peiiJnJinn.  Except  for  the  difference  in  size,  the  arrangement  of  the  vascular  bundles 
in  the  peduncle  and  their  structure  is  closely  similar  to  that  in  0.  pendulum. 

7 


THE    OPHIOGLOSSALES 


The  anatomy  of  O.  simplex,  so  far  as  it  has  been  investigated  (see  Bower  8) 
corresponds  closely  with  that  of  the  other  species  of  the  section  Ophioderma. 

The  roots  of  0.  pendulum  also  show  the  tetrahedral  apical  cell  (fig.  67),  but  the 

divisions  are  much  less  regular  than  in 
O.  moluccanum  and  probably  the  other 
species  of  the  Euophtoglosstim.  The 
segments  divide  slowly  and  increase  a 
good  deal  in  size  before  the  first  divi- 
sions take  place,  so  that  the  youngest 
segments  may  equal  the  apical  cell  in 
size,  and  there  is  thus  a  certain  resem- 
blance to  the  apical  meristem  in  the 
root  of  the  Marattiaceae.  It  is  prob- 
able that,  as  in  the  Marattiaceae,  the 
lateral  segments  of  the  apical  cell  also 
contribute  to  the  root  cap,  which  is 
rather  better  developed  than  it  is  in 
O.  moluccanum. 

There  is  a  good  deal  of  difference 
in  the  structure  of  the  root  bundle 
(fig.  68).  This  is  diarch  in  the  primary 
root,  as  we  have  seen,  and  also  in  the 
smaller  ones  of  older  sporophytes;  but 
in  the  larger  roots,  which  may  reach 
a  diameter  of  over  3  millimeters,  it  is 
triarch;  tetrarch  bundles  are  also  com- 
mon, and  in  one  very  large  root  which 
I  examined  the  bundle  was  pentarch, 
but  one  of  the  xylem  rays  was  shorter  than  the  others,  the  xylem  forming  a  solid 
central  mass  having  the  form  of  an  irregular  five-pointed  star. 


intermedium  Hk.,  slighlly 
a  very  much  reduced  1 


fragment 


99 


Material  was  lackiiiu  tor  a  snuU'  nf'rlu-  anat(iin\-  nC  rlu-  ilii/oim-  in  O.  />/jl>niitiirri 
(fig.  70),  but  tile  structure  dI  rlic  ])Lti()lL-  is  \  l  1  )•  iiurIi  like-  that  ot  O.  prnJuluNi  and 
probably  the  same  relation  of  the  leaf  bundles  to  the  bundles  of  the  rhizome  obtain 
as  in  O.  pendulum.  The  difference  in  the  venation  has  already  been  pointed  out 
and  the  leaves  differ  also  from  those  of  0.  pcnduluru  in  the  fact  that  stomata  are 
developed  only  upon  the  lower  side.  A  feature  of  this  species  is  the  presence  at  the 
base  of  the  leaves  of  very  conspicuous  multicellular  branching  hairs,  (juite  different 
from  those  found  in  any  other  species  of  Op/iioglossum  (fig.  70,  C).  I  find  that  the 
cells  are  much  more  elongated  in  my  specimens  than  those  figured  in  the  account 
of  the  ( )phioglossace.-i' given  in  the  Naturliche  Pflaii/enfamilien.* 

iiiK  si'okoi'iniK  OK  Korm-ciiu.M. 

There  is  much  the  same  uncertaint\-  as  to  the  iiumlnr  of  s|Hcics  iA'  Butix,  linnii 
that  there  is  in  Opiuoglossum.  Some  of  the  species  are  e.xceedingl)-  variable  and 
their  limits  are  difficult  to  determine.  Bitter,  in  his  account  of  the  Ophioglossace;c 
in  Engler  and  Prantl's  "Naturliche  Pflanzenfamilien,"  states  that  there  are  sixteen 
species.  Underwood  (Underwood  1)  says  "about  thirty,"  of  which  fifteen  occur  in 
the  United  States.    Christensen  in  his  Inde.x  Filicum  recognizes  thirty-four  species 

Many  of  the  species  are  very  widespread,  being  most  abundant  in  the  North 
Temperate  Zone.  According  to  Christ  (Christ  I),  B.  lunarta  is  not  only  widespread 
throughout  the  colder  parts  of  the  Northern  Hemisphere,  but  occurs  again  in  the 
corresponding  regions  of  the  Southern  Hemisphere,  having  been  reported  from  Pat- 
agonia, southern  Australia,  Tasmania,  and  New  Zealand.  A  few  species  occur  in 
the  mountain  regions  of  the  tropics;  thus  B.  laiuiginosum  is  not  uncommon  in  the 
highlands  of  Ceylon,  where  I  collected  it  at  an  altitude  of  about  7,000  feet. 

The  simplest  member  of  the  genus  is  Botrycluum  simplex,  a  very  variable 
species  occurring  at  various  places  in  Noith  America,  northern  Asia,  and  Kurope. 
Its  smaller  forms  closely  resemble  a  small  Opliioglossutii  (fig.  J2,A,  B),  except  that 
the  sporangia  are  more  distinct.  From  this  primitive  type,  obviously  not  very 
remote  from  Opiuoglossum,  there  is  an  interesting  series  of  forms  leading  up  to  the 
large  species  like  B.  virgiiiiatuim  and  B.  silatfohum.  This  latter  species,  which 
grows  in  the  mountains  of  western  North  America,  is  perhaps  the  largest  of  the 
genus  (plate  7).  The  plant  is  sometimes  2  feet  high,  the  leaf  nearh'  a  foot  in  width. 
and  the  very  large  panicle  of  sporangia  6  inches  01  more  in  length. 

In  the  evolution  of  the  leaf  in  Botrvrlinnu,  xhv  sjiorangiophort'  shows  a  devel- 
opment parallel  with  that  of  the  sterile  leaf.  In  the  forms  of  B.  simplex,  lia\ing 
an  entirely  undivided  sterile  lamina,  the  sporangiophore  has  the  form  of  a  simple 
spike  with  a  single  row  of  large  sessile  sporangia  on  either  side  (fig.  72,  J)  and  very 
closely  resembles  a  small  Opiuoglossum.  As  the  sterile  leaf  segment  becomes  more 
and  more  dissected,  there  is  a  corresponding  branching  of  the  sporangiophore  which, 

•  Prc.frssor  Biiwrr.  at  the  last  meeting  of  the  British  .Association  for  the  .Advanci-incnt  of  Science,  read  a  paper  on  the  Anatomy 
of  Ophiogloaum  pulmaiuiii.  This  has  not  yet  been  published,  but  Professor  Bower  has  kindly  furnished  me  with  an  abstract  of 
his  paper  from  which  the  following  extract  is  quoted. 

"It  was  thought  probable  that  0.  palmaium  (the  only  spiiies  .>(  Mction  (./le/Vojj/ojju)  would  share  with  the  species 
named  (i.e.,  the  species  of  Ofiluoderma)  the  character  of  a  d\\\A-  1 1 1  ii  1 1  i,  ,  in,l  material  collected  in  Jamaica  has  shown 
that  it  docs.     The  axis  is  much  distended  by  parenchymatcn;  i  nili  and  cortex,  and  as  a  consequence  the 

meshes  of  the  stele  arc  transversely  widened.  From  their  ni.ir  l  :  i  ;  ■  m  '  li  ti,  hut  not  quite  simultaneously,  arise  two 
strap-shaped  strands,  which  are  thus  widely  apart  in  their  on;;ni.  .\:ui  ui  .luibion  into  numerous  smaller  strands,  these 
range  themselves  into  two  fan-like  semicircles,  which  spread  till  tlicir  margins  meet,  forming  the  circle  of  strands  of  the 
petiole.  A  remarkable  feature  of  the  stock  is  the  intrusion  of  roots  into  the  bulky  pitli;  this  is  especially  obvious 
towards  the  base,  where  they  pass  out  as  thick  mycorrhizic  roots." 
This  behavior  of  the  roots  recalls  that  of  the  Ma 


100 


THE    OPHIOGLOSSALES 


in  the  large  forms  of  B.  virginianum  and  B.  sUaifoliiim,  forms  a  large  panicle  15 
centimeters  or  more  in  length  and  bears  many  hundred  sporangia.  Two  types  of 
leaf  division  may  be  noted,  a  pinnate  form  represented  by  5.  lunaria  and  its  allies, 
which  are  sometimes  separated  as  a  special  genus  Eiihotrychiiim,  and  a  ternate 
division  which  is  found  in  all  of  the  larger  species.  These  larger  species  form  a 
second  section,  Phyllotrichinm.  A  third  genus,  OsmunJopteris, has  been  proposed  to 
include  Botrychium  virginianum  and  its  allies.     In  most  of  the  species  of  Botrychium 


Ophioglosmm  simplex 
Ridley  (after  Bower). 
The  fertile  leaf  has  no 
sterile  lamina. 


Fig.  ^z.■ — (A-D,  after  Luerssen.) 
A,  B.  Botrychium  simplex  Hitchcock.     C,iS.  ternatum  S 
D,  B.  lunaria  (L.)  Swz.    E,  B.  virginianum  (L.)  Swz. 


PHE    ADULT    SPOROPHYTE 


101 


the  tcxnuc  (if  the  katis  soft  and  Hcsh}-,  like  that  of  Opiiioglossum,  hut  in  li.virgini- 
niiutn  it  is  thin  and  niemlManaceous,  hkc  that  of  many  true  ferns.  In  B.  limartn 
(fig.  72,  D)  the  venation  comes  nearer  to  that  of  Ophinglossum  than  is  the  case  in 
the  larger  species.  The  fan-shaped  leaflets  have  no  midrib  and  the  veins  branch 
dichotomously  from  the  base  of  leaf,  radiating  from  this  point  in  the  manner  de- 
scribed as  "cyclopterid."     In  the  larger  species  the  leaflets  have  a  distinct  midrib 


E.G.  73. 

A.  Rhizome  of  a  strong  plant  of  Botrychium  virginianum.     Xi.    The  base  of  the  expanded  le; 

B.  Section  of  the  terminal  bud.    j(,  stem  apex,    i,  n,  111,  the  three  youngest  leaves.     X2.66. 

C.  Section  of  petiole,  enlarged. 

D.  Section  of  rhizome;  p.pith;  m,  medullary  rays;  jr.xylem;  f  A,  phloem;  c,  cambium;  iA,endode 


A-G.  A  series  of  sections  of  the  sporophyll  of 

Botrychium  la, 

.ugSnosum  \\z 

position.    Csi-cticmof  pedunck-. 

H.  Section  of  the  petiole  of  the  cotyledon  of  B. 

virg^inianum.    i 

,  !,  lacuna:. 

and  the  forking  veins  are  attached  to  this  laterally  (fig.  72,  E).  The  type  of  B. 
lunaria  is  with<nit  question  the  more  primitive,  and  were  the  ends  ot  the  veins  united 
so  as  to  inclose  areoles  there  would  be  exactly  the  same  type  of  venation  as  is  found 
in  Ophioglossiini. 

In  Eiihotrychimn  the  anatomy  of  the  leaf  is  almost  exactly  like  that  of  Ophto- 
glossum,  stomata  being  developed  upon  both  sides  of  the  leaf;  the  mesophyll  is 
composed  of  absolutely  similar  cells  throughout  and  the  vascular  bundles  running 


102 


THE    OPHIOGLOSSALES 


through  the  mesophyll  do  not  project  at  the  surface  as  veins.  In  the  section  Phyllo- 
tric hi  um,  where  the  sterile  lamina  is  horizontal,  stomata  are  developed  only  upon  the 
lower  surface.  In  these  forms  the  mesophyll  is  more  compact  upon  the  upper  side, 
but  does  not  develop  a  distinct  palisade  layer.  The  epidermal  cells  may  be  simply 
elongated,  e.  g.,  B.  lanuginosum,  or  they  may  be  undulate,  e.  g.,  B.  virgtnianum. 
The  development  of  the  stomata  was  examined  in  B.  lanuginosum  and  the  stoma 
was  found  to  arise  directly  from  an  unmodified  epidermal  cell.  The  section  Eubo- 
trychium  shows  a  further  approach  to  Ophioglossum  in  the  character  of  its  stipular 
sheath,  which,  as  %ve  have  seen,  forms  a  hood-like  appendage  at  the  base  of  the  leaf, 
while  in  B.  virginianum  the  stipular  sheath  is  open  in  front,  so  that  there  are  really 
two  stipules.  Moreover,  the  leaf  in  the  latter  is  sharply  bent  over  in  the  bud  in  a 
way  to  suggest  somewhat  the  circinate  vernation  of  the  Marattiaceae.  For  the  most 
part  the  surface  of  the  plant  is  quite  smooth,  as  in  Ophioglossum,  but  the  sheaths 


Fig.  75. 

A.  Stem  apex  of  young  sporophyte  of  Botrychium  virginianum. 

B.  Cross-section  of  stem  apex. 

C.  Part  of  vascular  cylinder  of  stem,    pi,  phloem;   cam,  cambiut 

D.  Some  of  the  tracheids,  more  enlarged,  showing  bordered  pits. 


;,  apical  cell;  /,  youngest  leaf.   X 
i;  A'v,  xylem;  m,  medullary  ray. 


enveloping  the  young  leaves,  as  well  as  the  very  young  leaves  themselves,  are  often 
hairy,  and  in  a  very  few  species,  like  B.  lanuginosum,  long  and  slender  unicellular 
hairs  are  sparsely  scattered  over  the  surface  of  the  adult  leaf.  The  stem,  as  we  have 
seen,  is  always  an  upright  rhizome  and  usually  unbranched,  but  adventitious  buds 
may  be  developed  (see  Bruchmann  2).  These  adventitious  buds  may  develop  into 
lateral  branches.  In  one  specimen  of  5.  lanuginosum  examined  by  me  there  were 
two  equal  branches,  presenting  the  appearance  of  a  dichotomy,  but  a  careful  exam- 
ination indicated  that  the  original  apex  had  been  destroyed  and  that  these  two 
branches  were  lateral  shoots,  which  had  probably  arisen  as  adventitious  buds.  In 
Eubotrychium  the  leaves  are  arranged  spirally  upon  the  rhizome,  as  they  are  in 
Euophtoglossum.  This  is  also  true  of  certain  members  of  the  section  Phyllotrichium, 
but  others,  e.  g.,  B.  ternatum,  are  arranged  in  two  rows,  thus  suggesting  the  dorsi- 
ventral  arrangement  found  in  Helminthostachys. 

The  structure  of  the  adult  stem  does  not  differ,  except  in  size,  from  that  of  the 
younger  plants  already  described.  In  Eubotrychium  the  cambium  is  absent  and 
apparently  there  is  no  secondary  increase  in  diameter,  but  all  of  the  larger  species 
oi  Phyllotrichium  show  a  greater  or  less  developmentof  the  cambium,  which  we  have 


TlIK     ADL' 


103 


noted  in  the  bundle  of /i.  virgniiaiunn.  1  lie  position  ot  the  sporangiophoie  is  some- 
what different  in  different  species.  In  Eulxjiryduutn  it  is  attached,  as  a  rule,  close  to 
the  junction  of  the  sterile  lamina  and  the  petiole,  very  much  as  it  is  \n  Eiiophioglossum. 
In  B.  ternatum  and  B.  obliquum  the  long  peduncle  is  inserted  very  much  further 
down,  sometimes  almost  at  the  level  of  the  ground,  so  that  at  first  sight  the  spor- 
angiophore  seems  to  be  quite  independent  of  the  sterile  leaf.     In  B.  virgintanum 


of  the  prniarv  rrait. 

B.  Lmugniosuui  it  is  inserted  close  to  the  base  of  the  sterile  lamina  or  even 
above  its  base,  and  in  the  hitter  species  there  may  even  be  sometimes  a  second  spo- 
rangiophore  developed  on  the  fertile  leaf  above  the  insertion  of  the  primary  one. 

Certain  species  show  various  monstrosities,  this  being  particularly  the  case 
with  B.  luuaria.  In  such  forms  certain  of  the  segments  of  the  sterile  lamina  may  bear 
sporangia.     A  number  of  rluse  curious  forms  are  figured  by  Goebel  (Goebel  2). 


104  THE    OPHIOGLOSSALES 

In  fig.  73,  A,  is  shown  the  terminal  bud  of  a  strong  plant  of  B.  virginianum. 
The  base  of  the  oldest  leaf  is  cut  away  so  as  to  show  the  young  leaf  for  the  next 
year,  which  is  seen  to  be  strongly  bent  over,  and  the  young  leaf  segments  are  rolled 
inward  in  a  way  that  very  strongly  reminds  one  of  the  young  leaves  of  the  typical 
ferns.  The  young  leaf  is  covered  with  hairs.  The  roots  are  thick  and  fleshy,  prob- 
ably one  corresponding  to  each  leaf,  although  this  is  not  always  easy  to  determine. 
They  are  much  contracted  at  the  point  of  insertion.  The  roots  branch  freely,  the 
branching  being  monopodial,  thus  resembling  Ophioglossum  pendulum.  An  exam- 
ination of  the  section  of  the  bud  shown  in  fig.  73  shows  that  the  young  leaf,  which 
is  to  unfold  the  next  year,  is  already  well  advanced  and  the  formation  of  the  young 
sporangia  has  just  begun.  The  sporangiophore  is  also  evident  upon  the  leaf  for  the 
following  year,  and  the  leaf  which  is  to  unfold  in  the  third  year  can  be  recognized, 
but  its  parts  are  not  yet  differentiated. 

While  the  roots  branch  freely  in  B.  virginianum,  this  is  much  less  marked  in 
B.  lunaria.  In  large  plants  of  B.  lainiginosum  which  were  examined  somewhat 
carefully  it  was  found  that  the  roots  appeared  to  be  quite  unbranched,  although 
equaling  those  of  B.  virginianum  in  diameter  and  showing,  like  them,  a  similar 
tetrarch  structure  of  the  vascular  cylinder.  A  more  careful  examination  showed, 
however,  a  few  very  short  branches  on  some  of  the  roots,  but  these  were  rare.  It 
may  be  that  the  rudiments  of  these  lateral  roots  are  formed,  but  that  they  do  not 
develop,  and  in  this  respect  there  is  a  certain  resemblance  to  the  condition  which 
obtains  in  Helminthostachys. 

The  anatomy  of  the  roots  does  not  differ  from  that  of  the  younger  sporophyte 
already  described,  except  that  in  the  larger  specimens  the  roots  are  regularly  tetrarch, 
while  in  Euhotrychium  they  are  permanently  diarch. 

The  earlier  roots,  as  in  Ophioglossum,  have  a  tetrahedral  apical  cell  which  shows 
a  more  regular  segmentation  than  is  found  in  the  later  roots  and  in  these  earlier 
roots,  at  least  in  B.  virginianum,  there  seems  little  question  that  the  tissue  of  the 
root  cap  is  derived  entirely  from  the  outer  segments  of  the  apical  cell.  In  the  larger 
roots,  taken  from  the  older  sporophyte,  this  regularity  is  not  so  marked  and  it  is 
probable,  although  this  could  not  be  determined  absolutely,  that  the  lateral  seg- 
ments of  the  apical  cell  may  also  contribute  to  the  tissues  of  the  root  cap.  The 
regularity  of  the  segmentation  is  still  less  marked  in  the  later  roots  of  5.  obliquum. 
A  slight  development  of  periderm  may  be  seen  in  the  older  roots,  but  this  does  not 
form  a  continuous  layer,  being  developed  only  in  irregular  patches.  The  secondary 
increase  in  diameter  of  the  roots  is  apparently  due  almost  entirely  to  simple  enlarge- 
ment of  the  cortical  cells. 

THE  SPOROPHYTE  OF  HELMINTHOSTACHYS. 

While  Helminthostachys  differs  very  much  in  habit  from  the  other  Ophio- 
glossaceae,  it  nevertheless  shows  that  it  is  unmistakably  related  to  them  and  especially 
to  Botrychium.  The  dorsiventral  prostrate  rhizome  with  the  ample  palmately 
divided  leaves  give  it  a  very  individual  aspect,  but,  as  is  shown  from  a  study  of  the 
early  history  of  the  sporophyte  and  the  gametophyte,  there  is  no  question  that  it 
should  be  associated  with  the  Ophioglossaceae.  As  yet  but  a  single  species  is  gener- 
ally recognized,  which  grows  throughout  the  Indo-Malayan  region,  extending  from 
the  Himalayas  through  the  Malay  archipelago  to  northern  Australia  (plate  8). 

The  anatomical  details  of  the  adult  plant  have  been  very  thoroughly  investigated 
by  Farmer  and  Freeman  (Farmer  2),  and  from  a  comparison  of  the  structure  of  the 
adult  sporophyte  with  that   of  the  younger  stages  it  is    clear  that  the  essential 


THK    ADULT    SPOROPHYTE 


105 


characters  are  established  at  a  comparatively  early  period.  The  rhizome  Tfig.  79) 
has  the  leaves  arranged  in  two  rows  on  the  dorsal  side,  sf)mewhat  as  in  Ophioglossum 
pnidiiliim,  but  the  leaves  are  less  crowded  and  the  internodes  are  evident,  although 
less  marked  than  is  often  the  case  in  the  very  young  sporophyte.  The  youngest 
leaves,  still  inclosed  in  the  stipular  sheath  of  the  next  older  one,  are  conspicuous  as 
blunt  projections,  situated  between  the  apex  of  the  rhizome  and  the  first  expanded 
leaf.  As  the  leaf  breaks  through  the  stipular  sheath  of  the  next  older  one  the 
sheath  is  split  into  two  stipule-like  flaps,  which  much  resemble  superficially  the 
stipules  of  the  Marattiace;e.  From  near  the  base  of  the  leaves  on  the  flanks  of  the 
rhi/ome  and  belonging  to  the  ventral  portion  of  the  stem  there  arise  the  thick  fleshy 


A.  Sporophyll  of  Helnrinihostachysy  somewhat  redu 

B.  Base  of  sporangiophore,  about  natural  size. 

C.  Stoma.     X200. 


Four  sections  of  the  sporophyll  Fig.  3  passes 
through  the  base  of  the  spike,  spi  4,  section  of 
peduDcle  of  spike. 


roots,  which  resemble  those  of  the  other  Ophioglossaceae.  According  to  Prantl 
(Prantl  1)  and  Farmer  (Farmer  2),  the  roots  bear  no  definite  relation  to  the  leaf, 
and  the  number  as  a  rule  somewhat  exceeds  those  of  the  leaves.  The  roots  branch 
monopodially,  as  in  the  larger  species  of  Botrychium,  but  Farmer  states  that  the 
lateral  rudiments  often  prove  abortive,  or  fall  away  at  an  early  period,  so  that  the 
roots  are  apparently  unbranched.  This  behavior  recalls  the  condition  found  in 
Botrychium  latiuginosiiin. 

The  leaves  are  very  different  in  general  aspect  from  those  of  the  other  Ophio- 
glossaceae, but  are  really  not  very  different  in  their  method  of  branching  from  the 
ternate  forms  oi  Botrychium.  There  are  still  traces  of  the  three  primary  divisions 
of  the  first  leaves  which  undergo  subsequent  divisions,  so  that  the  leaf  has  a  palmate 
form  (plate  8,  B).    To  a  certain  extent,  however,  these  divisions  are  the  result  of 


106 


THE    OPHIOGLOSSALES 


unequal  dichotomy,  like  that  which  results  in  the  first  divisions  of  the  primary  leaves. 
In  large  plants  the  leaves  may  reach  a  length  of  30  or  40  centimeters.  The  petiole  is 
nearly  cylindrical  at  its  base,  but  higher  up  becomes  slightly  winged  at  the  margins, 
these  wings  passing  into  the  lamina.  A  section  of  the  petiole  taken  a  little  way 
below  the  insertion  of  the  sterile  lamina  shows  that  the  peduncle  of  the  sporangio- 
phore  is  recognizable  for  a  long  distance  below  the  point  at  which  it  becomes  free, 
its  adaxial  surface  projecting  as  a  rounded  ridge  between  the  wings  on  the  margin 
of  the  petiole  (fig.  78,  D).  In  texture  the  leaves  are  firmer  and  more  leathery  than 
in  any  of  the  other  Ophioglossaceae,  and  in  this  respect,  as  well  as  in  their  venation, 
they  closely  resemble  such  Marattiaceae  as  Dancea  and  Angiopteris. 

The  sporangiophore  is  to  some  extent  intermediate  in  character  between  that  of 
Ophioglossum  and  Botrychium.  It  is  inserted  near  the  junction  of  the  lamina  and 
petiole,  but,  as  already  stated,  can  be  traced  for  some  distance  below  the  point  where 
it  joins  the  petiole.  The  fertile  portion  of  the  sporangiophore,  which  may  reach  a 
length  of  nearly   10  centimeters,  is  composed  of  crowded,  short  branches,  upon 


which  are  borne  groups  of  nearly  globular  sporangia  much  like  those  oi  Botrychium. 
The  ends  of  the  branches  which  bear  the  sporangia  may  be  expanded  into  small  leaf- 
like organs  which,  under  exceptional  conditions,  look  much  like  small  leaves,  upon 
which  the  individual  sporangia  are  borne  (see  Bower  9,  fig.  239).  The  stem  in 
Helminthostachys  almost  always  remains  unbranched,  except  that  there  may  be 
formed  adventitious  buds  somewhat  as  in  Botrychium.  The  origin  of  these  buds, 
however,  has  not  been  investigated.  The  rhizome  is  rather  fleshy  in  texture  and 
may  reach  a  diameter  of  about  a  centimeter.  Usually  but  one  leaf  is  fully  developed 
at  a  time,  but  it  is  not  uncommon  to  find  two  leaves  produced  the  same  season. 
Farmer's  description  and  figures  of  the  structure  of  the  terminal  bud  show  that  it  is 
essentially  the  same  as  we  have  found  it  to  be  in  the  younger  plant,  and,  as  has 
already  been  pointed  out,  it  shows  strong  resemblances  to  the  terminal  bud  in 
Botrychium  lunaria. 

The  stomata  (fig.  78,  C)  are  confined  to  the  lower  surface  of  the  leaf  and  are 
surrounded  by  a  series  of  concentrically  placed  cells  like  those  around  the  stoma  in 
Ophioglossum  pendulum.     They  are  much  smaller  in  size,  however,  and  in  this 


THK    ADULT    Sl'UROl'HVTE  107 

resptct  ni;i\-  Intrn  lie  compaiiil  to  tlu-  stonKita  o{'  J)(in,rtu  oni.-  of  tlic  Marattia- 
cea?,  whicli  slmus  a  similar  lonccntiic  arrangement  ot  tlie  accessor)-  cells.  A 
cross-section  ot  the  leaf  shows  that  the  mesophyll  is  better  ditteientiatecl  than  in 
Botrychntru.  I  here  is  a  single  compact  layer  of  palisade  cells  below  the  epidermis, 
and  below  these  the  mesophyll  has  very  large  intercellular  spaces  which  communicate 
with  the  stomata.  In  the  anatomy  of  the  leaf,  therefore,  as  well  as  in  its  venation, 
Helmintliostiuliys  more  nearly  resembles  the  IVIarattiace;e  than  it  does  the  other 
Ophioglossace:e.  The  section  of  the  jHtioie  is  not  unlike  riiat  of  Ophio  gloss  urn 
pendulum  (figure  78,  D).  A  section  nuule  near  the  base  of  the  petiole  is  almost 
circular  in  outline  and  there  is  a  ring  of  separate  bundles.  On  the  adaxial  side, 
however,  two  other  bundles  are  seen  inside  the  outer  circle.  Farmer  and  Freeman 
(Farmer  2)  state  that  the  number  of  bundles  is  about  seven  or  eight,  but  the 
larger  specimens  which  I  have  examined  show  a  greater  number.  If  a  section  of 
the  petiole  is  examined  higher  up  it  no  longer  appears  circular,  but  is  slightly 
lobed,  these  lobes  corresponding  to  the  bases  of  the  three  divisions  of  the  sterile 
lamina,  and  on  the  adaxial  side  may  be  seen  a  fourth  lobe  which  marks  the  position 
of  the  peduncle  of  the  sporangiophoie.  In  this  upper  region  of  the  petiole  the 
bundles  become  more  or  less  coalescent.  but  two  adaxial  bundles  remain  quite 
distinct  and  are  continued  upward  into  the  spike.  The  structure  of  the  bundles  is 
concentric  and  the  general  appearance  of  the  section  is  quite  similar  to  that  found 
in  the  larger  species  of  Botrychiutn. 

The  anatomy  of  the  stem  in  the  older  sporophytc  does  not  differ  in  an)-  partic- 
ular, except  in  the  greater  size  of  its  parts,  from  that  of  the  sporophytes  already 
described.  The  vascular  cylinder  forms  a  hollow  tube  with  narrow  leaf  gaps  above, 
but  quite  solid  on  its  ventral  face.  Farmer  states  that  there  is  both  an  outer  and  an 
inner  endodermis  and  that  wood  is  formed  inside  of  the  protoxylem,  so  that  the 
bundle  is  mesarch. 

Reference  has  already  been  made  to  the  invaginated  canals  communicating  with 
the  stipular  cavities  and  first  described  by  Gwynne-Vaughn  (Gwynne-Vaughn  1). 
In  connection  with  these  he  describes  slight  projections  of  tissue  from  the  vascular 
cylinder,  which  are  surrounded  by  the  endodermis.  These  projections  he  thinks 
may  perhaps  be  the  vestiges  of  buds  whifh  formed  at  the  axils  of  the  leaves  and 
never  developed.  Whether  this  explanation  is  the  correct  one  or  not  there  is  no 
means  of  determining.  Farmer  found  in  the  older  plants  that  the  roots  were  prevail- 
ingly hexarch,  ranging  from  pentarch  to  heptarch,  and  that  tetrarch  roots  were  rare. 

The  endodermis  in  the  bundles  of  the  later  roots  is  much  less  distinct  than  it  is 
in  the  primary  root,  where  it  is  very  easily  demonstrated.  Within  the  endodermis 
is  a  layer  of  pericycle  cells,  separating  the  endodermis  from  the  radially  arranged 
masses  of  xylem  and  phloem.  Farmer  states  that  the  apical  cell  of  the  root  appears 
triangular  in  section  (presumably  in  longitudinal  section),  but  that  it  is  very-  often 
destroyed  and  as  a  result  of  the  proliferation  of  the  adjacent  tissue  an  area  of  cells 
results  recalling  the  condition  obtaining  in  the  Marattiacea?.  He  also  remarks  that 
most  of  the  roots  that  he  examined  showed  this  abnormal  condition. 

I  made  sections  of  a  number  of  roots  taken  from  young  sporophytes  where  the 
root  tips  appeared  to  be  (|uite  normal.  The  result  was  rather  interesting.  In  the 
early  roots  there  was  usually  present  a  tetrahedral  apical  cell,  very  much  like  that 
of  Botryrliiiini  and  showing  a  pretty  regular  segmentation  (fig.  80,  C).  The  seg- 
ments cut  ott  from  tlu  apical  cell  are  large,  and  even  in  the  early  roots  it  is  pretty 
certain  that  tin  root  cap  owes  its  origin,  in  part  at  least,  to  the  outer  cells  of  the  lateral 
segments.  Cross-sections  of  the  apical  cell  show  the  same  triangular  form  as  longi- 
tudinal sections  and  the  divisions  in  the  segments  of  the  apical  cell  seem  to  be  veiy 


108 


THE   OPHIOGLOSSALES 


much  as  they  are  in  Botrychtum.  In  one  small  root,  however  (fig.  80,  D),  the  apex 
was  occupied  by  three  cells  which  together  formed  a  triangular  group,  but  these 
cells  were  of  about  equal  size  and  it  is  not  at  all  certain  that  the  triangular  cell  x 
was  really  the  apical  cell. 

In  longitudinal  sections  of  the  larger  roots  there  is  a  close  approximation  of 
the  condition  found  in  the  Marattiaceae.  There  is  probably  still  a  single  apical  cell, 
as  there  is  in  the  early  roots  of  the  Marattiaceae,  but  this  cell  is  somewhat  truncate 
below  (fig.  53,  B)  and  in  a  cross-section,  taken  from  a  tetrarch  root,  a  single  apical 
cell  was  not  clearly  to  be  distinguished.    The  lateral  segments  are  very  large    and 


A.  Section  of  pentarch  root  of  Helminihoitachy 

B.  Part  of  the  vascular  bundle.     X150. 


C.  Root  of  young  sporophyte,  with  tetrahedral  apical  cell. 

D.  Root  of  an  older  .-sporophyte,  with  truncate  apical  cell. 


there  are  cut  off  from  them  cells  which  contribute  to  the  root  cap.  In  short,  the 
apical  growth  in  the  later  roots  of  Helminthostachys  is  evidently  more  like  that  of 
DancBa,  for  example,  than  it  is  like  Botrychtum. 

THE  SPORANGIOPHORE  OF  THE  OPHIOGLOSS./\LES. 

In  all  of  the  Ophioglossaceae  the  sporophyll,  as  we  have  seen,  consists  of  two 
parts,  the  fertile  spike  (or  sporangiophore)  and  the  sterile  lamina.  There  is  very 
great  diversity  of  opinion  as  to  the  real  nature  of  the  sporangiophore.  The  earlier 
views  were  strongly  influenced  by  the  old  theory  that  the  sporangial  parts  were 


TH1-:    ADULT    SPOROPHYTE  109 

secondary  modiHcations  of  an  originally  sterile  leaf.  At  present  it  is  the  belief  of 
most  students  of  the  ferns  that  the  fertile  structures  of  the  sporophyll  are  older  than 
the  sterile  ones,  and  this  has  led  to  a  quite  different  interpretation  of  the  real  nature 
of  the  fertile  segments. 

Bower  (Bower  9)  has  treated  at  length  the  different  theories  that  have  been 
proposed  to  explain  the  nature  of  the  fertile  spike  in  the  Ophioglossaceie.  We  can 
only  refer  briefly  to  some  of  the  more  important  of  these.  Mettenius  (Mettenius  1) 
considered  that  the  two  parts  of  the  leaf  were  of  equal  value,  but  he  gives  no  data 
as  to  their  origin.  Later  writers,  e.  g.,  Holle  (Holle  1),  Goebel  (Goebel  I),  and  very 
recently  Chrysler  (Chrysler  I),  consider  the  fertile  spike  to  be  the  equivalent  of  the 
fertile  pinnx'  of  such  a  fern  as  Aneimia.  Hplle  and  Chrysler  think  that  the  single 
median  spike  is  the  equivalent  of  two  united  pinn.ne.  Goebel  thinks  that  the  spike 
represents  a  single  pinna  which  has  arisen  in  a  median  position  instead  ot  upon 
the  margin.  Chrysler's  results  are  based  mainly  upon  a  study  of  the  distribution  of 
the  vascular  bundles  in  Botrychium.  His  results,  however,  do  not  take  into  account 
the  early  development  of  the  sporangiophore  and  its  relation  to  the  primordium 
of  the  very  young  fertile  leaf. 

Bower,  who  has  made  the  most  complete  study  of  the  development  of  the  spore- 
bearing  parts  in  the  Ophioglossaceae  that  has  yet  been  published,  concluded  in  his 
earlier  work  that  the  spike  of  Ophioglossum  is  morphologically  equivalent  to  the 
single  sporangium  of  Lycopodium.  In  this  view  he  was  supported  by  Strasburger 
and  Celakovsky  (Celakovsky  1).  More  recently,  however,  he  has  modified  his  view 
(Bower  9)  and  concludes  that  the  sporangial  spike  is  a  distinct  organ,  for  which  he 
suggests  the  name  "sporangiophore."  This  later  interpretation  we  believe  to  be 
the  correct  one. 

In  Ophioglossum  the  sporangiophore  develops  a  peduncle  which  is  often  very 
much  longer  than  the  sterile  portion  of  the  leaf  and  forms  much  the  most  conspicuous 
portion  of  the  sporophyll  (fig.  55).  The  fertile  portion  of  the  sporangiophore  is  a 
flattened  spike  along  whose  margins  the  two  rows  of  large  sporangia  are  borne. 
These  project  very  little,  the  cavity  of  the  sporangium  being  deeply  sunk  in  the  tissue 
of  the  spike  and  covered  by  several  layers  of  cells  forming  the  outer  wall  of  the  spor- 
angium. The  number  of  the  sporangia  in  a  spike  may  be  only  six  or  seven  in  some 
of  the  small  forms  of  Euophioglossiim,  or  it  may  be  very  large,  as  it  is  in  the  great 
spikes  of  0.  pendulum. 

In  0.  pendulum  and  O.  intermedium  the  spike  is  more  flattened  than  it  is  in  the 
species  of  Euophtoglossum  and  the  central  sterile  portion  is  wider  in  proportion. 
Stomata  are  almost  entirely  absent  from  the  epidermis  of  the  spike  in  O.  pendulum, 
although  occasionally  a  few  are  found  in  the  central  region.  In  O.  intermedium 
they  are  more  numerous  than  in  O.  pendulum,  but  much  less  abundant  than  in  the 
species  of  Euophtoglossum.  In  the  latter  they  may  occur  even  upon  the  epidermis 
of  the  wall  of  the  sporangium.  The  most  marked  exception  in  the  position  of  the 
sporangiophore  is  seen  in  the  section  Cheiroglossa  (plate  5).  In  this  form  there  are 
several  sporangiophores  developed  upon  the  leaf.  Although  these  are  apparently  mar- 
gmal  in  position,  it  is  claimed  by  Bower  that  they  are  really  always  developed  upon 
the  adaxial  surface  of  the  leaf.  Some  of  the  smaller  forms  may  show  a  single  spike 
which  occupies  a  central  position,  very  much  like  that  of  O.  pendulum   (plate  5,  3). 

In  some  of  the  simpler  forms  of  Botrvehinm  simplex  the  sporangiophore  is  very 
much  like  that  of  a  small  Ophioglossum,  except  that  the  individual  sporangia  are 
more  distinct,  although  the  base  of  the  sporangium  is  coherent  with  the  margin  of 
the  sporangial  spike.  In  all  of  the  other  species  of  Botrychium,  however,  the  spor- 
angiophore branches,  the  degree  of  branching  following  very  closely  that  of  the 


no 


THE    OPHIOGLOSSALES 


Sterile  lamina.  In  the  larger  species,  like  B.  virginianiim,  many  hundred  sporangia 
may  be  developed  upon  a  single  sporangiophore.  In  these  larger  and  more  special- 
ized forms  the  sporangium  is  usually  smaller  and  is  better  difFerentiated,  always 
having  a  more  or  less  distinct  pedicel. 

The  form  of  the  sporangiophore  in  H ehnnithostach\s  is  to  some  extent  inter- 
mediate between  that  of  Ophioglossum  and  Botrychium,  but  on  the  whole  comes 
nearer  to  Botrychium.  The  sporangia  are  densely  crowded  along  the  flanks  of  the 
spike,  thus  forming  two  rows  somewhat  as  in  Ophioglossum,  but  they  are  very  much 
more  crowded  and  are  formed  in  groups  or  synangia  which  project  free  above  the 
surface  of  the  young  spike.  The  sporangia  do  not  arise  singly,  but  are  borne  upon 
short  branches  or  secondary  sporangiophores  which  suggest  the  lateral  branches  of 
the  sporangiophore  in  Botrychium,  but  are  far  less  regularly  disposed.  By  the  fur- 
ther growth  of  the  sporangia  the  axis  of  the  spike  is  entirely  concealed  and  a  casual 
examination  would  indicate  that  the  sporangia  were  formed  equally  at  all  points  of 
its  surface,  but  a  study  of  the  development  shows  that  they  are  lateral  in  structure, 
as  they  are  in  Ophioglossum. 

THE  DEVELOPMENT  OF  THE  SPORANGIOPHORE. 

The  sporangiophore  in  both  Ophioglossum  and  Botrychium  becomes  visible  at 
a  very  early  period.  In  Ophioglossum  moluccainnn  I  have  found  that  the  spor- 
angiophore can  be  recognized  even  earlier  than  Bower  has  stated  for  0.  vulgatum 
and  O.  rcticulatum.  A  median  section  of  a  very  young  fertile  leaf  in  0.  moluccaiium 
is  shown  in  fig.  56,  D.     The  apex  of  the  leaf  has  scarcely  become  free  and  the  apex, 

as  well  as  nearly  the  whole  of  the 
adaxial  surface,  is  made  up  of 
large  columnar  meristem  cells,  of 
which  it  is  difficult  to  say  that 
any  one  is  the  single  apical  cell 
of  the  leaf.  The  leaf  trace  is  al- 
ready evident,  passing  into  the 
base  of  the  young  leaf,  which  is 
strongly  inclined  forward  so  that 
the  real  apex  of  the  leaf  is  not 
directed  vertically  upward,  but  is 
on  the  adaxial  side  of  the  leaf 
rudiment.  The  apex  of  the  young 
sporangiophore  arises  from  the 
tissue  immediately  below  the  apex 
of  the  sterile  segment,  and  the 
whole  of  the  adaxial  portion  of 
the  leaf  below  the  apex  of  the 
young  sporangiophore  may  be  said 
to  belong  to  the  latter  and  not 
to  the  sterile  portion  of  the  leaf. 
There  is  thus  practically  a  dichot- 
omy of  the  apex  of  the  young 
sporophyll,  and  the  two  branches  (viz,  the  sterile  segment  and  the  sporangiophore) 
are  structures  of  equal  rank.  It  would  thus  appear  that  the  old  view  put  forward 
by  Mettenius  of  two  equal  branches  of  the  fertile  leaf  is  probably  the  correct  one. 
It  is  probable  that  younger  stages  than  those  figured  by  Bower  for  O.  vulgatum  and 
0.  reticulatum  would  show  the  same  condition  of  affairs  that  we  pointed   out  in 


A.  Longitudinal  section  of  young  sporophyll  of  Ofihioglos. 

still  inclosed  in  the  stipular  sheath,  sh     X50. 

B.  Apex  of  sterile  lamina,     sp,  sporangiophore. 

C.  .^pel  of  sporangiophore.      X125. 

D.  Transverse  section  of  a  very  young  sporophyll,  showing  di< 

apex.     X125. 


THK    ADULT 


11] 


O.  tnoliiiirinuin  and  O.  />riuli/li<ni,  and  flu-  conclusion  that  the  young  sporangiophore 
is  an  outgrowth  of  the  sterile  part  of  the  leaf  is  the  result  of  the  subsequent  rapid 
growth  of  the  upper  sterile  portion  of  the  leaf,  which  thus  carries  its  apex  far  beyond 
the  apex  of  the  young  spike. 

The  young  sporophyll  in  O.  />rn  Julian  (hg.  64,  K)  resembles  that  of  0.  moluc- 
canum,  except  that  all  the  parts  are  much  larger.  Ihe  apex  of  the  young  sporangio- 
phore appears  upon  the  adaxial  side  of  the  very  broadly  conical  young  sporophyll. 

Bruchmann's  studies  on  Botrxchium  lunaria  indicate  that  in  this  species  the 
separation  of  the  fertile  and  sterile  segments  of  the  sporophyll  is  the  result  of  a 
diciiotomv  of  the  apex  of  the  sporophvli  at  a  very  early  stage  in  its  development. 


in  Opluoolosstim 
ic  ha\e  not  been 


A.  Young  sporophyll  of  Ophiogloimm  prmliilum.   sp,  llic  sporangiopliorc 

B.  An  older  sporophyll.     Xi. 

C.  A  still  older  stage,  showing  venation  of  lamina. 

D.  Base  of  a  full-grown  sporangiophore. 
K.  Sporophyll  with  rudimentary  lamina,  /. 

The  sporoph}ll,  however,  is  larger  at  this  time  than  is  the  case 
moluccamtni  (Bruchmann  2,  fig.  57). 

The  earliest  stages  in  the  development  of  the  sporangioph( 
studied  in  Hclninithostachys.     Bower  says  (Bower  9,  page  455): 

"The  origin 
unlike.       It  appe; 
frond,  and   it  is 
downward." 

In  the  latter  respect  it  might  ver\-  well  be  compared  to  the  stronglv  bent-ovi 
sporangiophore  of  Botrychiiini  virgiiiiaiiinn. 


)f  it  is  similiar  (i.  e.,  to  Ophtoglossum)  and  its  early  stages  not 
rs  at  first  as  an  outgrowth  on  the  adaxial  side  of  the  sterile 
urved    over  while   youn<i   so   that   the   actual   apex   is    pointed 


112  THE    OPHIOGLOSSALES 

After  the  separation  ot  the  fertile  and  sterile  portions  of  the  sporophyll  the 
sterile  segment  at  first  grows  much  more  rapidly  than  the  sporangiophore  and  soon 
extends  beyond  it,  so  that  the  sporangiophore  has  the  appearance  of"  being  merely 
an  adaxial  appendage  of  the  sporophyll.  These  changes  in  the  relative  importance 
of  the  points  can  be  very  well  shown  by  a  study  of  the  very  large  sporophylls  of  0. 
pendulum.  In  this  species  the  young  leaf  emerges  from  the  sheath  while  it  is  still  in 
a  very  early  stage  of  development.  These  young  leaves  (fig.  82)  have  a  very  thick, 
fleshy  leaf  base,  ending  in  the  small  pointed  lamina,  bent  over  and  almost  hiding  the 
young  sporangiophore  which  is  attached  to  its  inner  surface.  This  curved-over 
form  of  the  young  sporophyll  differs  from  that  oi  Eiiophioghssum^  where  the  young 
leaf  is  straight,  and  in  this  respect  there  is  a  suggestion  of  Botrychiiim  or  of  the 
true  ferns.  The  young  spike  at  this  stage  is  almost  equal  in  length  to  the  sterile 
lamina. 

If  the  very  young  sporophyll  of  Ophioglossum  mohiccatium  is  examined,  it  will 
be  seen  that  the  vascular  bundle  leaving  it  passes  downward  and  joins  a  young  root 
trace.  Very  soon  after  the  bundle  enters  the  young  leaf  it  divides  into  two  branches, 
one  of  which  passes  into  the  base  of  the  spike  and  the  other  and  larger  one  into  the 
sterile  section  of  the  sporophyll.  This  latter  bundle  now  divides  again  into  two, 
one  of  which  passes  to  the  dorsal  side  of  the  sterile  segment  while  the  other  is  turned 
toward  the  ventral  side  of  the  leaf,  which  probably  represents  tissue  belonging  to  the 
sporangiophore.  In  the  cross-sections  of  older  leaves  the  petiole,  which  includes 
the  completely  fused  base  or  peduncle  of  the  sporangiophore,  shows  three  distinct 
bundles,  a  large  abaxial  one  and  two  smaller  adaxial  bundles.  The  former  remains 
undivided  for  some  distance  above  the  base  of  the  insertion  of  the  peduncle  of  the 
sporangiophore.  The  two  adaxial  bundles  divide  into  several  branches,  this  begin- 
ning just  below  the  point  where  the  lamina  of  the  sterile  leaf  becomes  differentiated 
from  the  petiole.  The  lamina  has  its  edges  infolded  so  that  it  has  a  conical  form, 
open  in  front  and  inclosing  the  young  spike  (figs.  56,  57).  The  successive  branching 
of  the  two  adaxial  bundles  follows  in  quick  succession,  and  the  outer  bundles  con- 
tribute to  the  veins  of  the  lamina;  the  inner  ones  pass  upward  into  the  peduncle 
of  the  spike. 

In  a  previous  paper  (Campbell  7)  the  conclusion  was  reached  from  the  study  of 
a  series  of  sections  at  different  heights,  taken  from  the  full-grown  sporophyll,  that 
the  two  adaxial  bundles  belonged  exclusively  to  the  spike.  A  study  of  the  devel- 
opment of  the  young  sporophyll  shows  that  this  statement  is  not  entirely  correct 
and  that  a  considerable  part  of  the  vascular  system  of  the  sterile  lamina  owes  its 
origin  also  to  branches  from  the  two  adaxial  bundles  before  the  latter  enter  the 
peduncle  of  the  sporangiophore.  Of  the  two  adaxial  bundles,  one  represents  the 
original  bundle  of  the  sporangiophore  derived  from  the  primary  forking  of  the  leaf 
trace;  the  other  is  derived  secondarily  from  a  subsequent  division  of^  the  second 
branch  of  the  leaf  trace,  this  also  giving  rise  to  the  large  abaxial  bundle  of  the  petiole. 

THE  DEVELOPMENT  OF  THE  SPORANGIUM. 

Much  the  most  complete  account  of  the  development  of  the  sporangium  of  the 
Ophioglossace^e  is  that  of  Bower  (Bower  5),  who  has  made  a  very  exhaustive  exam- 
ination of  the  development  of  the  sporangium  in  all  three  genera.  My  own  studies 
have  been  for  the  most  part  confined  to  Ophioglossum  pendulum,  O.  moluccanum, 
and  Botrychium  vtrginiariurn.  Burlingame  (Burlingame  1)  has  more  recently 
examined  the  development  of  the  sporangium  in  a  species  of  Ophioglossum  from 
the  Philippines,  which  was  assumed  to  be  O.  reticulatum.  Beers  (Beers  1)  has- 
also  published  recently  a  somewhat  incomplete  account  of  the  sporangium  in  Hel- 


THK    ADULT    SI'OROl'H  ">  ll-.  113 

nnlwstaclixs.       I'lin.iiuli  the  kiiuiiKss  of  Prof.  1,.  L.  Biulingame   1   havi-  also  had 
soiiif  of  his  |->ie|iaiations  ot  OpIiKJi^lossitm  nin  iil/iturn  and 


an  opportunity  to  exanmu- 
Helmtnthostach  ys. 

An  examination  of  hotli  lonijitiidinal  and  cross  sections  ot  the  \()un<i  s|)ike  in 
().  ttiohiirtiinttn  (and  this  is  true  also  of  O.  piiululum)  shows  that  they  agree  entirely 
account  of  the  de\elopnient  in  the  species  studied  by  him.     There 


ith   H< 


.A.  'I'ransvcrse  i.cction  of  a  very  young  sporangiophore  of  Ophioglos!um  moluccnnum.     X  1 50. 

B.  Section  of  an  older  sporangicphore.      X75.      The  shaded  areas  mark  the  "  sporangiogenit "  hands. 

C.  Part  of  B,  more  highly  magnified.    The  nucleated  cells  mark  the  sporangial  region. 

seems  to  be  no  question  that,  as  Bower  first  pointed  out,  there  is  formed  a  continuous 
band  of  tissue  on  each  side  of  the  sporangiophore,  this  band  being  the  so-called 
"sporangiogenic"  band,  from  which  the  individual  sporangia  are  differentiated 
later.  The  sporangia  arise  from  this  sporangiogenic  band  at  more  or  less  definite 
intervals,|  these  fertile  areas  being  separated  by  bands  of  sterile  tissue.  In  the 
sporangial  areas  periclinal  walls  are  formed  by  which  an  inner  mass  of  tissue,  the 


Development  of  the  sporangium  in  Opiiioglassum  prnJu< 
spt  sporogenous  tissue.  A  is  a  longitudinal  section; 
mature  sporangia.    X8. 

archesporium,  is  separated  from  the  outer  cells  which  are  to  form  the  wall  of  the 
future  sporangium.  The  inner  cells  constituting  the  archesporium  later  give  rise 
to  the  masses  of  spores.  Between  the  young  sporangia  there  lie  partitions  or  septa 
formed  from  the  intei-vening  sterile  cells  of  the  sporangiogenic  band.  The  cell 
groups  which  form  the  archesporia  and  the  sterile  septa  are  derived  from  sister  cells 


114 


THE    OPHIOGLOSSALES 


of  the  original  sporangiogenic  bands.  Bower  thinks  that  all  of  the  sporogenous 
tissue  can  not  be  traced  back  to  a  single  primary  archesporial  cell,  and  that  spore- 
bearing  tissue  is  formed  secondarily  by  periclinal  divisions  in  the  cells  outside 
of  the  original  archesporium.  In  some  of  the  very  young  sporangiophores  of  O. 
pendulum  there  can  sometimes  be  seen  a  single  large  epidermal  cell  which  may 
possibly  be  the  mother  cell  of  a  young  sporangium,  but  it  is  very  difficult  to  determine 
this  point  satisfactorily. 

After  the  archesporium  is  differentiated  there  is  a  rapid  division  in  its  cells  and 
there  is  thus  formed  a  very  large  mass  of  cells,  whose  limits,  however,  are  not  always 
very  clearly  marked.  Later  on  the  contents  of  these  cells  become  denser  and  are 
more  easily  distinguished  from  the  surrounding  sterile  tissue. 

The  cells  lying  outside  the  archesporium  divide  rapidly  both  by  longitudinal 
and  transverse  walls  and  give  rise  to  the  thick  outer  wall  of  the  sporangium.  In  lon- 
gitudinal sections  through  the  sporangium  two  rows  of  cells  may  be  seen  extending 
from  the  mass  of  archesporial  cells  to  the  outside  of  the  sporangium.  These  two 
rows  of  cells  mark  the  point  where  the  transverse  cleft  arises  by  which  the  spo- 
rangium opens  at  maturity.    The  outer  cells  derived  from  the  archesporial  complex 


A,  B.  Young  sporangia;  C,  an  older  sporangium  of  Boirychwm  vugummu 

tissue  is  shaded;   the  nucleated  cells  adjoining  form  the  tapetum. 

do  not  develop  into  spores,  but  constitute  the  tapetum,  which  later  becomes  dis- 
organized and  forms  a  sort  of  plasmodium  extending  among  the  growing  spore 
mother  cells,  and  is,  no  doubt,  of  great  importance  in  the  further  development  of 
these.  Bower  thought  that  some  of  the  inner  cells  of  the  archesporial  tissue  contrib- 
uted to  this  Plasmodium,  but  a  further  study  has  led  him  to  the  conclusion  that  this 
is  not  the  case  and  that  all  of  the  inner  cells  of  the  archesporium  develop  into  spores. 
This  view  is  confirmed  by  the  recent  paper  of  Burlingame  (Burlingame  I),  who 
investigated  the  development  of  the  spores  in  O.  reticulatum. 

At  maturity  the  sporangium  opens  by  a  transverse  cleft  whose  position  is  already 
evident  in  the  younger  stages  of  the  sporangium.  As  the  cells  shrink  with  the  drying 
of  the  ripe  sporangium  the  spores  are  crowded  out  through  this  cleft,  but  there  is 
no  special  mechanism  like  the  annulus  found  in  the  sporangia  of  the  higher  ferns 
which  facilitate  the  dispersal  of  the  spores. 

Our  knowledge  of  the  development  of  the  sporangium  of  Botrychium  has  been 
based  largely  upon  the  study  of  5.  lunaria.  I  have  investigated  with  some  care  the 
development  in  B.  virginianum,  which  differs  mainly  from  B.  lunaria  in  the  smaller 


115 


rh;ir  it  has  a  wull-nuirkfd  thougli  sliort  indicil. 
7/,  siuh  as  B.  siriiplf.x,  rht-  sporangia  are  nuich 


■lopnifiit  ot  the  indiviclual 


ingia  hegin; 


si/e  of  the  spoiangiimi  aiul  the  tan 
In  the  simplest  forms  of  Botryrhni 
larger  and  are  sessile. 

In  B.  virginiatiurn  (rig.  85)  the 
just  about  a  year  previous  to  their  ripening,  and  if  the  plants  are  taken  up  about  the 
time  the  spores  are  shed  the  earliest  stages  of  the  sporangia  will  be  found  in  the  leaf 
which  is  to  expand  the  following  season.  At  this  time  the  sporangiophores  in  the 
larger  specimens  are  thrice  pinnate,  and  the  youngest  recognizable  sporangia  are 
borne  at  the  tips  of  the  branches.  These  young  sporangia  form  slight  elevations 
which  become  smaller  as  they  approach  the  tip  of  the  segments,  and  if  an  exact 
median  section  is  made  of  one  of  these  young  sporangia  it  will  be  seen  to  have  at  its 
apex  a  large  pyramidal  cell  with  a  truncate  base.  Holtzman  (Holtzman  1),  states 
that  the  whole  sporangium  may  be  traced  back  to  a  single  cell  and  that  the  divisions 
at  rirst  are  like  those  of  a  three-sided  apical  cell.  I  have  not  been  able  to  satisfy 
myself  as  to  the  accuracy  of  this  statement,  but  the  youngest  stages  which  I  have 
been  able  to  find  would  not  forbid  such  an  interpretation,  although  there  seems  no 
question  that  the  basal  part  of  the  sporangium  is  derived,  in  part  at  least,  from  the 
surrounding  tissue. 


Fig.  S6. 
Sporangiophores  of  Helmwihosiachys.  The  two  lower  figures  seen  from  above.    /,  sterile  appendages.     X3. 
Section  of  a  young  sporangium,  showing  sporogenous  tissue,  sp;  tapetum,  /;  and  wall.  rr.     (From  preparation 
made  by  Prof.  L.  L.  Burltngame.) 


.  Section  of  a  young  spora__„ , ,__ 

lade  by  Prof.  L.  L.  Burltngame.) 

The  terminal  cell  of  the  sporangium  is  divided  b\  a  periclinal  wall  into  a  single 
inner  cell  which  forms  the  archesporium,  and  an  outer  one  which  contributes  to  the 
wall  of  the  sporangium.  The  outer  cell  rapidly  divides  and  similar  divisions  occur 
in  the  archesporium.  H\  active  growth  in  the  basal  part  of  the  sporangium  it  pro- 
jects more  and  more  until  it  assumes  the  form  of  a  projecting  globular  body  with  a 
short  stalk,  thus  diffViing  stiikingK  fiom  the  deeply  sunken  sporangia  of  Ophio- 
olcissiirn.  It  is  impossible  to  detect  an\  difinire  succession  of  divisions  in  the  arche- 
sporium, which  ultimateh-  becomes  changed  into  a  large  globular  mass  of  cells  with 
the  usual  dense  contents,  separated  from  the  outside  of  the  sporangium  by  half  a 
dozen  or  more  layers  of  sterile  cells.  The  cells  immediately  adjoining  the  sporo- 
genous tissue  constitute  the  tapetum.  Bower  states  that  the  tapetum  is  exclusively 
derived  from  this  outer  sterile  tissue,  but  it  must  be  said  that,  in  Botrycluutn  vir- 
giniamim  at  least,  the  limits  between  the  sporogenous  tissue  and  the  tapetum  are  by 
no  means  easy  to  detect.  The  wall  of  the  ripe  sporangium  has  tVom  four  to  six 
layers  of  cells  and  the  dehiscence  is  by  a  vertical  cleft,  whose  position  may  sometimes 


116  THE    OPHIOGLOSSALES 

be  recognized  in  the  young  sporangium  by  cells  arranged  very  much  as  they  are  in 
the  sporangium  oi  Ophioglossiim.  The  stalk  is  traversed  by  a  short  vascular  bundle 
which  can  first  be  recognized  v^^hen  the  sporogenous  cells  are  pretty  well  advanced 
in  their  development. 

The  sporangia  of  Helmintlwstachys  on  the  whole  more  resemble  those  of 
Botrvchium  than  those  of  Ophioglossurn.  In  the  very  young  sporangiophore  there 
is  developed  a  band  of  tissue  on  either  side  much  like  that  in  Ophioglossurn  (see 
Bower  9,  page  455).  Transverse  sections  of  the  fertile  spike  show  that  the  spo- 
rangiophores  originate  from  certain  groups  of  cells  of  this  sporangiogenic  band. 
These  young  sporangiophores,  however,  project  above  the  surface  and  later  form 
crowded  projections  which  may  undergo  a  greater  or  less  degree  of  branching,  so 
that  the  number  of  sporangia  borne  upon  a  single  one  of  these  secondary  sporangio- 
phores may  be  considerable.  These  sporangiophores  become  irregularly  lobed  and 
the  final  divisions  of  these  develop  into  the  sporangia  in  a  manner  which  is  very 
similar  indeed  to  that  of  Botrvchium,  but  the  individual  sporangia  are  usually  less 
distinct.     Bower's  account  of  the  further  development  may  be  quoted  as  follows: 

"It  has  already  been  noted  that  the  position  and  number  of  the  sporangia 
which  they  bear  are  inconstant.  In  earl}'  stages  it  is  impossible  to  distinguish 
the  cells  which  will  give  rise  to  the  sporangia,  but  from  rather  older  stages  it  ap- 
pears that  the  sporogenous  groups,  together  with  the  superficial  cells  which  cover 
them  are  referable  in  origin  to  the  segmentation  of  a  single  superficial  cell.  More- 
over, the  first  periclinal  division  of  the  cells  defines  the  whole  of  the  sporogenous 
tissue  from  the  protective  wall.  As  the  sporangia  grow  older  the}'  project  from 
the  surface  of  the  sporangiophore.  The  sporogenous  mass  increases  rapidly  in 
bulk,  while  the  cells  surrounding  the  sporogenous  mass  to  the  extent  of  several 
layers  assume  the  character  of  a  tapetum  which  gradually  becomes  disorganized; 
finall)'  the  sporogenous  cells  separate  and  divide  into  tetrads.  As  the  sporangia 
approach  maturity  the  upper  part  of  the  sporangiophore  may  grow  out  into  an 
irregular  rosette  of  laciniae  of  vegetative  tissue." 

A  study  of  the  older  sporangia  oi  Hehninthostachys  shows  that  the  tapetum  is 
extraordinarily  developed,  constituting  a  very  thick  layer  surrounding  the  mass  of 
spores  (fig.  86).  The  clusters  of  fully  developed  sporangia  are  often  very  regular 
in  form  (fig.  86,  A),  and  remotely  suggest  the  synangium  of  a  Marattiaceous  fern. 


Part  II.  THE   MARATTIALES. 

The  members  of  the  second  order  of  the  Eusporangiatae — the  Marattiales — 
resemble  quite  closely  the  typical  Leptosporangiatae.  Both  in  the  form  and  venation 
of  the  leaves  and  in  the  development  of  the  sporangia  upon  their  lower  surface  they 
recall  the  common  ferns.  But  the  structure  of  the  sporangium  is  very  different, 
and  both  in  its  structure  and  development  the  sporangium  shows  certain  evident 
resemblances  to  that  of  the  Ophioglossaceae. 

The  Marattiaceous  type  is  a  very  old  one,  and  this  fact  lends  a  special  interest 
to  these  few  survivors  of  the  ancient  Paleozoic  fern  flora.  Like  the  Ophioglossaceae, 
the  leaves  of  the  Marattiace;c  are  thick  and  fleshy  in  texture,  but  usually  firmer  than 
is  the  case  in  the  Ophioglossaccae.  Some  of  the  smaller  species  oi  Dana-a  are  only 
2  or  3  decimeters  in  height,  but  the  larger  species  of  Marattia  and  Angiopteris  are 
among  the  largest  of  the  ferns.  The  latter,  which  is  common  in  the  eastern  tropics 
and  e.xtends  to  Australasia,  is  a  noble  fern  whose  great  caudex,  covered  with  the 
persistent  leaf  bases,  is  nearly  as  big  as  a  barrel,  and  the  gigantic  leaves  reach  a 
length  off  or  6  meters,  with  stalks  almost  as  thick  as  a  man's  arm.  In  the  dense, 
wet  forests  of  Tjibodas  in  Java,  for  example,  the  development  of  this  fern  is  espe- 
cially luxuriant,  and  groups  of  them  form  one  of  the  most  striking  features  of  this 
rich,  tropical  flora. 

The  Marattiacea?  frequent,  for  the  most  part,  the  moist,  shady  forests  of  the 
tropics,  where  they  form  a  characteristic  feature  of  the  vegetation.  Along  the  steep 
banks  of  moist,  shady  ravines  or  streams  they  sometimes  occur  in  profusion. 

The  number  of  living  Marattiaceae'-'  is  small,  some  authorities  recognizing 
only  about  thirty  species.  There  is,  however,  a  good  deal  of  difference  of  opinion 
as  to  the  number  of  species  in  some  of  the  genera.  This  is  especially  true  of 
Angiopteris,  which  many  authorities  consider  to  have  only  one  single,  extremely 
variable  species,  while  others  recognize  many  species.  One  of  the  genera,  Marattia, 
is  widespread  throughout  the  tropics  of  both  hemispheres,  where  there  are  about  25 
species.  (See  Bitter  I,  Christensen  1.)  One  of  these,  M.  iloiiglasii,  extends  to  the 
Hawaiian  Islands,  where  it  is  a  common  and  conspicuous  fern.  Angtoptcris  is 
widespread  throughout  the  tropics  of  the  old  world  and  reaches  beyond  the  tropics 
into  Australia  and  southern  japan.  Archangiopteris,  with  a  single  species,  A. 
henryi,  is  a  recently  discovered  form  occurring  in  southwestern  China.  Kaidfussta, 
also  a  monotypic  species,  occurs  throughout  the  Indo-Malayan  region  and  extends 
as  far  as  the  Philippines.  The  genus  Danwa  is  exclusively  neo-tropical  and  com- 
prises about  20  to  25  species,  most  of  which  occur  in  the  West  Indies,  northern 
South  America,  Central  America,  and  Mexico.  A  sixth  genus,  Macroglossinii,  from 
Borneo,  has  recently  been  described  (Copeland  1). 

Of  these,  Kaiilfussia  is  the  most  aberrant,  differing  markedly  from  the  other 
genera  in  the  form  and  venation  of  the  leaves,  as  well  as  in  the  shape  and  position 
of  the  synangia.  Kaiilfussia  and  most  species  of  Daiicra  have  dorsiventral  rhizomes, 
while  the  other  genera  have  an  upright,  radially-constructed  caudex. 

The  gametophyte,  in  all  of  the  investigated  species,  is  a  large,  dark-green, 
fleshy  thallus,  much  resembling  superficially  such  a  liverwort  as  Prllia.  1  he  re- 
productive organs  are  very  much  like  those  of  Ophioglossum,  and  chlorophyll  is 
formed  in  abundance  in  the  gametophyte.     The  large  liverwort-like  gametophyte 

*  Christensen  (I)  recogniics  6i  species  of  Angiopteris,  i  of  Archangiopteris,  26  of  Danata,  i  of  Kaulfussia,  and  z8  of  Marattia. 

117 


118  THK    MARATTIALES 

and  the  character  of  the  reproductive  organs  are  marked  indications  of  the  primitive 
nature  of  these  ancient  ferns.  The  embryo  also  shows  many  points  in  common  with 
that  of  the  Ophioglossaceae.  As  in  the  latter,  the  organs  of  the  young  sporophyte 
are  all  of  epibasal  origin  and  the  vascular  system  in  the  young  sporophyte  belongs 
exclusively  to  the  leaf  and  root,  the  stem  being  entirely  destitute  of  a  proper  stele. 

In  Dancsa  a  short  suspensor  is  usually  developed,  but  the  other  genera  have  as 
yet  shown  no  examples  of  this. 

The  sporophyte  is  very  much  alike  in  its  early  development  in  all  of  the  Marat- 
tiaceae.  The  young  plant  consists  at  first  mainly  of  the  primary  leaf  and  root,  which 
are  traversed  by  a  single  axial  vascular  strand  as  in  Oplnoglosstini  mohiccanum,  but 
a  stem  apex  is  developed  at  an  early  period,  although  it  remains  relatively  incon- 
spicuous. 

Kaiilfussia,  Danaa,  and  ArcJiangtopteris  are  all  ferns  of  moderate  size  and 
comparatively  simple  structure  ;  but  Marrattia,  Angiopteris,  and  Macroglossum 
are  very  large,  and  the  arrangement  of  the  vascular  bundles  in  the  stem  becomes 
exceedingly  complex,  corresponding  to  the  numerous  bundles  in  the  enormously 
developed  leaves. 

The  form  of  the  leaf  in  the  Marattiace?e  ranges  from  a  perfectly  simple  leaf  in 
Dancea  simpJicifoUa  to  the  gigantic  decompound  leaves  oi  Angiopteris  and  Marattia. 
Most  of  the  species  oi  Datura  (and  this  is  true  also  oi  Archangiopteris  and  Macro- 
glossum) have  simply  pinnate  leaves,  while  in  Kaulfussia  the  leaves  are  palmately 
divided  into  from  three  to  seven  leaflets,  the  larger  leaves  looking  curiously  like  a 
horse-chestnut  leaf  in  outline,  whence  the  specific  name.  The  ternate  form,  which 
is  often  found  in  Kaulfussia,  recurs  in  the  early  leaves  of  the  other  genera  and  is 
sometimes  retained  in  quite  large  leaves  in  Marattia  (plate  12,  B).  This  recurrence 
of  the  ternate  leaf  form  suggests  Helminthostachys  and  the  ternate  species  of 
Botrvtliiiim.  The  leaves  are  usually  quite  smooth,  but  in  the  earlier  stages  there  is 
sometimes  a  sparing  development  of  hairs  and  scales.  The  latter  are  especially- 
noticeable  upon  the  leaves  of  the  young  sporophyte  in  Dancea. 

The  leaves  are  furnished  at  the  base  with  very  conspicuous  fleshy  stipules 
which  remain  adhering  to  the  stem  after  the  leaves  fall  away,  and  these  leaf  bases, 
with  their  attached  stipules,  more  or  less  completely  cover  the  surface  of  the  stem. 
As  the  leaves  fall  away  they  leave  a  characteristic  scar  marked  by  the  remains  of  the 
vascular  bundles.  The  leaf  base  as  well  as  the  stalks  of  the  leaflets  shows  a  more  or 
less  marked  enlargement,  recalling  the  pulvinus  which  occurs  so  commonly  in  the 
Leguminosae.  It  is  at  this  point  that  the  leaf  stalk  separates,  the  smaller  divisions 
of  the  leaf  often  breaking  away  from  the  main  or  secondary  rachis,  in  the  same 
fashion  as  the  main  leaf  stalk  falls.  In  the  large  species  of  Marattia  and  Angiop- 
teris this  enlarged  leaf  base  with  the  two  thick,  fleshy  stipules  curiously  resembles 
in  shape  and  size  the  hoof  of  a  horse. 

The  leaves  when  young  are  coiled  up  in  the  same  fashion  as  those  of  the  typical 
ferns  and  their  venation  in  general  is  decidedly  fern-like,  the  ultimate  veins  being 
dichotomously  branched  and  the  venation  very  much  like  that  of  Helniinthostachys 
or  certain  species  of  Botrychiuni.  In  Kaulfussia,  however,  the  venation  is  reticulate 
and  strikingly  like  that  of  the  typical  Dicotyledons.  In  its  earlier  stages,  however, 
there  is  a  marked  resemblance  to  the  venation  of  Ophioglossum. 

The  fleshy  leaves  do  not,  as  a  rule,  show  a  very  large  development  of  mechanical 
tissues;  but  there  is  developed,  especially  in  the  larger  leaves,  a  thick  layer  of  hypo- 
dermal  tissue,  which  is  usually  sclerenchyma,  somewhat  like  that  of  the  typical  ferns, 
but  may  be  thick-angled  tissue  or  collenchyma,  such  as  is  common  in  many  flow- 
ering plants.     A  marked  anatomical  feature  is  the  presence  of  large  mucilage  ducts. 


THK  c;amktophvtf  119 


I.    I  UK  GAMK'rOPHVri;. 


The  first  account  of  the  germination  and  development  of  the  gametophyte 
in  the  Marattiaceae  was  published  by  Luerssen  (Luerssen  2),  who  studied  the 
germination  in  Marattia  cicuta-foUa  and  in  Angtopterts.  Not  long  afterward  the 
Dutch  botanist,  Jonkmann,  published  an  account  of  the  development  of  the  prothal- 
lium  in  both  Marattia  and  Atigioptens.  His  original  paper  (published  in  Dutch, 
but  afterward  translated  into  French)  gives  an  extremely  satisfactory  account  of  the 
germination  and  development  of  the  prothallium  and  reproductive  organs  (Jonk- 
mann 1).  Somewhat  later  he  also  published  a  preliminary  account  of  the  germina- 
tion in  Kaulfussia,  but  apparently  the  work  was  never  published  in  full  (Jonkmann 
2).  In  1892  Farmer  (Farmer  I)  described  the  gametophyte  and  embryo  in  Angi- 
opteris  evecta  and  in  1894  the  writer  (Campbell  3)  gave  an  account  of  the  prothallium 
and  embryo  in  Marattia  donglasii  collected  in  Hawaii.  Two  years  later  Brebner 
(Brebner  2)  described  the  prothallium  and  embryo  in  Daticea  simplicifolta.  In 
1908  the  writer  published  an  account  of  the  prothallium  and  young  sporophyte  of 
Kaulfussia  (Campbell  9)  and  in  1909  a  preliminary  note  was  published  in  regard 
to  Daiia-a  (Campbell,  10). 

The  following  account  of  the  germination  is  based  mainly  upon  the  work  of 
Jonkmann.  I  have,  however,  examined  the  early  germination  stages  in  Marattia 
douglasii  for  comparison  with  Jonkmann's  account,  and,  so  far  as  my  experiments 
went,  it  agrees  entirely  with  the  species  described  by  Jonkmann. 

The  ripe  spores  of  the  Marattiaceae  are  small  and  may  be  either  of  the  bilateral 
type  or  tetrahedral  (radial).  According  to  Jonkmann,  the  bilateral  spores  are  much 
more  abundant  in  Marattia  than  the  radial  spores,  but  in  Aiigiopteris  the  radial 
spores  predominate.  The  wall  of  the  spore  (see  Jonkmann  I,  pp.  203,  204)  shows  a 
differentiation  into  an  inner  membrane  orendospore  and  a  middle  layer,  the  exospore, 
which  is  often  found  divided  into  layers.  There  is  a  very  thin  external  coat,  the 
perispore  or  epispore,  which  is  generally  thrown  off  in  the  early  stages  of  germination 
or  even  before  germination  begins.  All  of  the  membranes  except  the  epispore  are 
colorless,  while  the  latter  is  a  more  or  less  pronounced  yellowish  brown  tint.  The 
surface  of  the  spore  is  roughened  by  small  papillae, which  arise  from  the  exospore. 
The  spores  contain  no  chlorophyll,  but  there  is  a  considerable  amount  of  oil  present, 
which  appears  as  drops  of  varying  size,  and  there  are  also  other  granular  contents — 
starch  and  albuminous  granules.  The  nucleus  lies  in  the  center  of  the  spore  and 
is  connected  with  the  peripheral  protoplasm  by  delicate  protoplasmic  filaments. 
Germination  begins  quite  promptly  under  favorable  conditions  and  within  about 
a  week  the  spores,  which  hitherto  were  quite  colorless,  begin  to  show  a  greenish 
tint,  due  to  the  development  of  chlorophyll.  Jonkmann  states  that  the  chlorophyll 
appears  first  as  flocculent  masses  near  the  nucleus,  but  these  apparently  amorphous 
masses  are  really  composed  of  very  small,  faintly  tinted  chromatophores,  which  lie 
between  the  large  oil  drops  and  rapidly  increase  in  size  and  depth  of  color  as 
germination  proceeds,  their  number  increasing  by  the  usual  division.  The  chloro- 
plasts  later  become  very  conspicuous  and  are  distributed  in  the  periphery  of  thenow^ 
very  much  enlarged  spore,  the  outer  membranes  of  which  are  ruptured  so  as  to 
expose  the  endospore,  containing  the  nucleus  and  numerous  large  and  conspicuous 
chloroplasts.     Starch  granules  are  also  to  be  seen  in  most  cases. 

The  cell  remains  undivided  until  it  has  attained  a  size  many  times  greater  than 
that  of  the  spore.  The  first  division  wall,  which  is  formed  about  a  month  after  the 
spores  are  sown,  is  transverse  both  in  Angtopterts  and  Marattia,  and,  like  that  in 
the  germinating  spore  of  Ophioglossum,  divides  the  primary  cell  into  two  nearly 


120  THE    MARATTIALES 

equal  parts  (fig.  87,  A).  A  rhizoid  may  be  cut  oft'  either  before  or  after  this  first 
transverse  wall  is  developed,  but  frequently  no  rhizoids  are  formed  until  a  much 
later  period,  as  in  Ophioglossum.  The  primary  rhizoid,  when  present,  is  formed 
much  as  in  the  typical  ferns,  the  papilla  from  which  it  develops  being  cut  off"  from 
the  larger  cell,  and  it  contains  little  or  no  chlorophyll.  F^ach  of  the  primary  prothal- 
lial  cells  divides,  in  typical  cases,  by  a  longitudinal  wall,  so  that  the  young  gameto- 
phyte  consists  of  four  cells,  arising  quadrant-wise  (fig.  88,  A),  and  closely  resembling 
corresponding  stages  in  Ophioglossum,  except  for  the  absence  of  chlorophyll  in  the 
latter.  Where  the  young  plants  are  crowded  or  light  is  deficient,  as  for  instance 
when  the  germination  occurs  within  the  sporangium,  there  is  a  tendency  to  the 
development  of  a  filament,  a  phenomenon  often  met  with  also  in  the  typical  ferns. 
Usually  one  of  the  upper  pair  of  cells  in  the  four-celled  stage  assumes  the  role 
of  an  apical  cell,  and  for  some  time,  as  in  the  typical  ferns,  there  is  growth  from  a 
two-sided  apical  cell  (fig.  88,  C).    As  soon  as  the  apical  cell  is  established,  it  grows 


A.  Two  germinating  spores  of  Mar. 

B.  Young  gametophyte  of  same  spe 

C.  Marattia  sambucina  Blume.  X 
D-H.  M.  douglmii  Baker.  D-F, 
D  and  E  represent  the  same  prothall 


i  jraxinea  Smith.    X200.     The  rem 
.     X75.     (.^,  B,  after  Jonkmann). 


very  much  as  it  does  in  such  a  liverwort  as  Aneiira  and  produces  a  thallus  of  the 
same  form  and  structure.  But  as  the  prothallium  grows  older  a  periclinal  wall 
is  formed  in  the  apical  cell,  and  in  the  outermost  of  the  two  cells  thus  produced 
there  is  a  longitudinal  wall  dividipg  it  into  two  equal  cells,  and  from  this  time  on 
it  is  impossible  to  recognize  a  single  apical  cell  in  the  prothallium,  the  apex  of  which 
is  occupied  by  a  group  of  apparently  similar  marginal  initial  cells. 

At  first  the  prothallium  has  a  spatulate  form,  but  before  the  single  apical  cell 
is  replaced  by  the  group  of  marginal  initials  the  outer  cells  of  the  younger  segments 
grow  more  rapidly  than  the  inner  ones,  so  that  they  project  beyond  the  apical  cell, 
which  thus  comes  to  lie  in  a  depression  between  the  two  lobes,  and  the  familiar 
heart-shaped  form  so  commonly  found  in  the  prothallium  of  most  ferns  is  established. 
The  marginal  initial  cells  vary  in  number  with  the  width  of  the  depression  in  which 
they  lie.  In  a  horizontal  section  they  appear  oblong  in  form,  but  in  the  vertical 
sections  made  they  have  a  semicircular  outline  (fig.  88,  D,  E). 


THE    GAMETOI'HYTI 


121 


liasal  segments  are  cutoff  by  a  wall  extending  the  wliolc  depth  of  the  piothalliuni 
and  the  segment  thus  cut  off  is  divided  at  once  by  a  horizontal  wall  into  a  dorsal  and 
ventral  cell  of  nearly  equal  size  (fig.  88,  E,  d,  v).  Cell  divisions  are  more  active  in  the 
ventral  segments,  more  manifestly  so  at  some  distance  back  from  the  apex.  It  is  due 
to  this  more  active  cell  division  in  the  ventral  segments  that  the  strongly  projecting 
cushion-like  mass  of  tissue  is  formed  upon  the  ventral  surface  of  the  prothallium, 
upon  which  the  archegonia  later  make  their  appearance.  The  superficial  cells  of 
both  surfaces  of  the  prothallium  have  a  thick  cuticle  which  often  makes  it  difficult 
to  embed  the  prothallia  without  bad  shrinkage.  From  the  under  side  of  the  prothal- 
lium nimierous  rhizoids  are  developed,  which  in  the  case  o{ Marattia  and  Angiopieris 
are  unicellular  and  thin-walled,  but  in  DiuKra  become  divided  into  several  cells. 
Sometimes  there  seems  to  be  no  definite  apical  growth  in  the  early  stages,  but  on  the 
other  hand  Jonkmann  states  that  both  of  the  superior  cells  may  function  as  apical 
cells,  thus  inaugurating  the  early  dichotomy  of  the  young  prothallium,  and  even  a 
third  branch  may  arise  from  one  of  the  inferior  (]uadrants,  which  assumes  the 
character  of  a  third  apical  cell. 

Among  the  leptosporangiate  ferns,  the  forms  which  most  nearly  resemble  the 
Marattiacese  in  the  development  of  the  gametophyte  are  the  Osmundaces,  especially 


the  genus  Osmunda  (Campbell,  Mosses  and  Ferns,  2d  ed.,  pp.  347,  348).  In 
Osmunda  there  is  often  a  tendency  also  to  the  formation  of  a  massive  structure  at  an 
early  stage  in  the  development,  due  to  the  formation  of  cell  divisions  in  three  planes, 
so  that  the  prothallium  becomes  from  the  first  more  than  one  cell  thick.  This 
tendency  in  the  Marattiaceae  becomes  much  more  pronounced  as  the  gametophyte 
grows  and  very  soon  there  is  evident  a  very  thick  midrib,  which  often  becomes 
exceedingly  conspicuous  in  the  older  gametophyte,  unlike  the  typical  ferns,  where 
the  thickening  of  the  prothallium  is  confined  to  the  region  which  bears  the  arche- 
gonia. In  the  Marattiace;e  this  thickening  extends  almost  to  the  margin  of  the 
prothallium,  so  that  it  is  only  at  the  extreme  edge  that  the  prothallium  shows  but  a 
single  layer  of  cells.  The  very  old  prothallia  in  Marattio  branch  dichotomously 
(fig.  87,  E,  E),  and  the  process  is  entirely  similar  to  that  found  in  manv  thallose 
liverworts.  The  original  growing  point  becomes  divided  by  the  development  of  a 
median  lobe,  thus  inaugurating  two  growing  points,  and  the  midrib  hack  of  tin- 
growing  point  forks  in  exactly  the  same  way  as  in  many  liverworts. 

Besides  this  dichotomous  branching,  it  is  not  at  all  uncommon  to  have  adven- 
titious buds  developed  upon  the  margin  of  the  thallus.    These  form  small  secondary 


122  THE    MARATTIALFS 

piothallia,  which  may  be  detached  and  become  independent  plants;  or  reproduc- 
tive organs  may  be  developed  upon  them,  usually  only  antheridia,  while  they  are 
still  connected  with  the  mother  plant.  The  prothallia  are  very  long-lived  and 
apparently  may  grow  indefinitely  so  long  as  the  archegonia  are  not  fecundated.  I 
kept  prothallia  of  Marattia  doiiglasii  for  nearly  two  years,  during  which  time  they 
grew  vigorously  and  finally  reached  a  length  of  over  2  centimeters.  At  the  end  of 
two  years  there  was  no  indication  of  the  slightest  decrease  in  their  vigor. 

The  prothallia  are  monoecious,  although  it  is  not  uncommon  to  find  small 
prothallia  which  bear  only  antheridia.  They  are  very  deep  green  in  color,  which 
together  with  their  more  massive  texture  makes  them  easily  distinguishable  from  the 
prothallia  of  the  ordinary  ferns,  and  they  very  often  look  more  like  such  a  liverwort 
as  Pellta  or  Anthoceros.  The  prothallium  of  A ngtopteris  very  closely  resembles  that 
of  Marattia,  but  is  often  somewhat  shorter.    The  difference  in  shape  in  the  prothallia 

of  the  form  studied  by  [onkmann  (//. 
pruuiosa  var.  hypoleiica)  and  the  Cey- 
lonese  form  studied  by  Farmer  and  my- 
self may  be  taken  as  an  argument  in  favor 
of  recognizing  a  specific  difference  between 
these  two  forms. 

The  archegonia  in  both  Marattia  and 
_  Angiopteris,  so  far  as  my  own  observations 

Fig.  89.  extend,  are  confined  to  the  lower  surface 

Two  gametophytes  of  Angiopieris  with  young  sporophyte      of  the  midrib.     Tonkmann,  howcver,  States 

attached,    em,  embryo;    cot,  cotyledon.  X^.  ,  •  ii       i  i  i  i 

that  occasionally  he  observed  archegonia 
developed  upon  the  upper  surface  as  well.  The  antheridia,  while  more  abundant 
upon  the  lower  surface  of  the  prothallium,  are  quite  commonly  met  with  also  upon 
the  upper  surface  and  are  not  restricted  to  the  midrib,  but  may  be  found  quite  near 
to  the  margin.  The  rhizoids  in  both  Angiopteris  and  Marattia  are  probably  always 
unicellular,  and  their  walls,  which  are  quite  strongly  cutinized,  are  dark  brown  in 
color. 

THE  PROTHALLIUM  OF  KAULFUSSIA.* 

The  prothallia  of  Kaulfiissia  are  usually  much  larger  than  those  of  either 
Marattia  or  Angiopteris.  They  are  very  massive,  strongly  resembling  a  Pellia  or 
Aneura.  The  specimens  described  here  were  collected  in  Java  in  a  small  ravine 
near  the  foot  of  the  volcanic  mountain  Salak.  The  youngest  prothallia  found 
were  about  5  millimeters  in  length  and,  like  the  older  ones,  were  decidedly  elon- 
gated, with  a  deep  sinus  in  front  (fig.  90,  A,  B).  There  were  a  few  antheridia 
occupying  the  forward  part  of  the  thick  midrib,  which  is  very  largely  developed 
in  Kaulfiissia,  as  it  is  in  the  other  Marattiaceae.  The  older  prothallia  are  relatively 
somewhat  broader  and  these  larger  ones  usually  bear  archegonia.  Only  in  a 
few  cases  were  young  antheridia  found  upon  the  prothallia  with  the  archegonia. 
Whether  this  is  always  true  could  not  be  decided  from  the  small  number  of  prothallia 
found.  The  antheridia  in  Kaulfiissia  seem  to  be  strictly  confined  to  the  lower  sur- 
face of  the  midrib  and  occupy  much  the  same  position  that  the  archegonia  do. 
After  the  antheridia  have  matured  and  discharged  the  speimatozoids,  archegonia 
arise  in  the  same  position  in  regard  to  the  apex.  Unlike  most  ferns,  the  walls  of  the 
empty  antheridium  do  not  become  discolored,  so  that  they  are  easily  overlooked. 
Careful  examination  of  the  sections  of  the  older  prothallia,  however,  will  almost 
always  show  the  empty  antheridia  and  it  is  probable  that  the  prothallia  are  usually 


'  Kauljussia  Blume  =  Ch 


THE    GAMF.TOPHYTF 


123 


pioteiandrous  aiul  not  did'cioiis.  as  might  be  siippostd  from  a  casual  examination. 
I'he  margins  of  the  large  prothallium  are  more  or  less  irregularly  lobed  and  it  is  not 
unlike  that  of  Osnunuhi,  but  as  in  the  other  Marattiace;c  the  wings  of  the  prothal- 
lium are  several  cells  in  thickness  near  the  midrib,  and  only  at  the  extreme  edge 
are  they  reduced  to  a  single  cell  in  thickness. 

rhe  full-grown  prothallia  are  a  centimeter  or  more  in  length  and  nearly  as 
bioad.  One  very  large  specimen  was  found  (fig.  90,  /■ ).  1  his  b;)re  a  young  sporo- 
phyte  with  two  fully  developed  leaves,  and  the  prothallium  measured  nearly  2.5 
centimeters  in  length  by  1.75  in  extreme  width,  and  was  also  very  thick.  A  second 
archegonial  cushion  was  present,  but  whether  this  was  due  to  a  forking  of  the  original 
apex,  such  as  not  uncommonly  occurs  in  Marattia  and  Angiopteris,  was  not  deter- 
mined, although  this  was  very  probably  the  case. 


B.  Apex  of  A,  showing  the  anthcridia,   f^      X20. 

C.  An  older  gametophyte,  with  archegonia,  V.     X4 

D.  Apical  region  of  an  older  gametophyte;  a-,  apical  cell. 

E.  An  older  gametophyte,  with  young  sporophyte  attached. 


ityledon; 


F.  Two  views  of  a  large  gametophyte,  with  attached  sporophyte,  natural  size. 

G.  Rhizoid.     X50. 

H.  Apex  of  rhizoid,  more  highly  magnified.    A  single  nucleus  only  is  present. 

The  rhizoids  are  stout  and  they  have  thick  but  quite  colorless  walls.  They 
o'^ten  show  apparently  transverse  septa  and  the  extremity  is  not  infrequently  forked 
(fig.  go,  H).  An  examination  of  these  rhizoids  shows  that  these  septa  are  not  the 
result  of  true  cell  division,  as  only  one  nucleus  can  be  found  in  the  whole  rhizoid. 
As  the  nucleus  is  large  and  conspicuous,  and  only  one  can  be  seen,  it  looks  as  if  the 
formation  of  septa  is  secondary  and  not  connected  with  cell  division.  The  structure 
of  the  apex  of  the  prothallium  is  exactly  as  in  Marottia  and  Augioptens.  The 
apical  meristem  shows  the  usual  row  of  marginal  initial  cells,  of  which  one  (fig.  90, 
D,  v)  is  often  somewhat  larger  than  the  others  and  may  possibly  represent  a  single 
apical  cell. 


124 


THE    MARATTIALES 


THE  PROTHALLIUM  OF  DAN^.A. 

In  July,  1908,  the  prothallia  of  three  species  oiDancea  were  collected  in  Jamaica. 
As  the  genus  Damea  has  received  comparatively  little  attention,  especially  as  regards 
the  gametophyte,  it  seemed  very  desirable  to  secure  as  complete  a  series  of  the  pro- 
thallia and  young  sporophytes  as  could  be  done,  and  to  this  end  the  trip  was  made 
to  the  West  Indies.  The  genus  Dancea  is  confined  to  the  American  tropics  and 
comprises,  according  to  Christensen,  26  species  of  extremely  characteristic  ferns. 
The  type  is  evidently  an  old  one,  as  some  of  the  fossil  Marattiaceae  are  closely  allied 
to  the  living  genus  Dana-a  and  may  possibly  be  referred  to  it.  The  only  account  of 
the  prothallium  hitherto  published,  so  far  as  I  am  aware,  is  the  paper  of  Brebner 
(Brebner  2)  on  D.  simplicifolia,  a  species  from  British  Guiana. 

In  1897  I  collected  a  small  number  of  specimens  of  prothallia  oi  Dantea,  prob- 
ably D.  jenmani,  and  in  the  summer  of  1 908  the  same  locality  was  visited,  as  well 
as  some  others  in  the  same  district,  and  material  of  three  species  was  secured.    These 


A.  Three  gametophytes  of  Danaa  jenmani  Underwood.     X2. 

B.  Three  young  gametophytes  of  D.jamaicensis  Underwood.     X4. 
C  Four  large  gametophytes  of  D.jamaicensis.    X2. 

0,1,  shows  four  groups  of  archegonia,  ? . 


collections  were  all  made  in  the  vicinity  of  Cinchona,  a  mountain  station  at  an  eleva- 
tion of  about  5,000  feet.  As  I  have  found  in  collecting  other  Marattiaceae,  the  most 
favorable  collecting  ground  for  the  prothallia  is  upon  moist,  clayey  banks  where  the 
fruiting  plants  are  growing.  In  the  shady  crevices  in  such  positions  a  careful  search 
will  usually  be  rewarded  by  the  discovery  of  numerous  young  plants,  and  with  these 
there  are  often  associated  prothallia  in  various  stages  of  development.  Brebner 
described  the  prothallia  of  D.  simplicifoUa  as  being  nearly  circular  in  outline,  but 
very  few  of  the  prothallia  of  the  species  collected  by  me  showed  this  form;  but  they 
were  usually  decidedly  elongated,  sometimes  very  strongly  so,  and  were,  as  a  rule, 
very  much  larger  than  the  specimens  of  Z).  simplicifoUa  described  by  Brebner. 

The  three  species  collected  by  me  were  D.  jamaicensts  Underwood,  D.  jenmani 
Underwood,  and  D.  elliptica  Smith.  In  all  three  species  the  larger  prothallia  are 
usually  decidedly  elongated  and  very  irregular  in  outline,  often  showing  conspicu- 
ous leaf-like  marginal  lobes,  like  those  occurring  in  the  prothallia  of  0.rmtiwi/a  and 
Gleichenia. 


THE    GAMETOPHYTE 


125 


The  germination  of  the  spores  and  the  early  stages  are  quite  unknown  in 
Daritta,  but  probably  resemble  those  of  the  other  genera  which  have  been  studied. 
To  judge  from  the  younger  stages  collected,  there  is  a  good  deal  of  variety  of  form, 
as  is  the  case  also  in  the  other  Marattiacea;.  The  youngest  specimens  collected 
belonged  to  D.  jamaicensis.  These  were  very  broad  in  outline  and  unsymmetrical, 
one  wing  of  the  prothallium  being  much  better  developed  than  the  other  (fig.  91,  B). 


Fig.  92  shows  some  older  specimens  of  Z).  clhptica  which  were  greatly  elongated, 
the  very  much  attenuated  posterior  region  being  quite  thin  and  delicate  in  texture, 
with  no  midrib  and  the  archegonial  cushion  being  confined  to  a  small  region  just 
back  of  the  growing  point.  The  marginal  region  in  these  young  prothallia  was 
composed  of  a  single  layer  of  cells  and  a  considerable  portion  was  made  up  of  but 


liyte,  probably  developcil  from 
X20.     rf  antheridia. 

B.  Large  qametophyte  of  D.  flliptica,  with  two  sporophytcs. 

C.  Multicellular  rhizoid.      Xioo. 

D.  A  cell  of  the  rhizoid,  showinR  nucleus,  n.     Xzio. 


bud  of  Dntura  janitiitftis 


two  layers,  while  the  mid  region,  where  the  antheridia  and  later  the  archegonia  are 
developed,  was  not  more  than  four  to  five  cells  in  thickness.  In  general  the  prothallia 
of  Daticea  are|lmore  delicate  in  texture  than  those  of  the  other  Marattiace;e  that 
have  been  studied. 


126 


THE    MARATTIALES 


A  midrib  usually  begins  to  form  at  an  early  period  and  in  the  older  prothallia 
may  become  very  conspicuous,  sometimes  reaching  a  thickness  of  eight  to  ten  cells. 
The  margin,  as  we  have  seen,  is  always  more  or  less  irregular  in  outline  and  often 
develops  large  leaf-like  lobes  which  are  particularly  conspicuous  in  D.  jamaicensis 
(fig.  91,  C),  but  are  noticeable  also  in  the  other  species.  The  large  prothallia,  which 
are  sometimes  nearly  3  cm.  in  length,  are  often  branched  (fig.  92,  D);  the  branching 


B,  antheridium  of   Maratlia  douglaiii.     tij  neck  ( 
i>,  ventral  canal  cell ;  o,  egg;  m,  mantle  celli. 


is  sometimes  unmistakably  a  true  dichotomy,  but  again  it  seems  to  be  adventi- 
tious. In  one  large  prothallium  of  £).  jamaicensis  of  very  irregular  form,  four  groups 
of  archegonia  were  present,  widely  separated  from  each  other.  It  could  not  be  cer- 
tainly determined  whether  these  arose  from  a  repeated  forking  of  the  original  apex 
or  whether  one  or  more  of  them  was  of  adventitious  origin  (fig.  91,  C). 


The  ape.x  of  the  prothallium  in  the  younger  stages  is  usually  uuknted  by  a 
sinus,  but  in  the  older  ones  the  heart  shape  is  almost  completely  lost  and  the  apex 
may  even  project  as  a  rounded  protuberance,  bearing  the  archegonia  upon  its  lower 
surface,  or  it  may  be  fan-shaped,  with  little  or  no  indentation  at  the  growing  point. 

The  prothallium  is  the  usual  dark-green  color  found  in  the  other  Marattiacea?, 
but  as  we  have  seen  is  rather  more  delicate  in  texture.  Of  the  three  species 
examined,  Dana-a  elUptica  resembles  more  nearly  the  prothallia  of  the  other  Marat- 
tiaceae  in  the  thickness  of  the  central  portion,  which  may  show  from  eight  to  ten 


12: 


layers  of  cells,  ihe  form  aiul  division  of"  the  apical  cells  is  exactly  the  same  as  in 
the  other  Marattiacea-.  Stiff  brown  rhizoids  are  developed  upon  the  lower  surface 
and  are  mainly  confined  to  the  midrib,  over  which  they  may  be  evenly  distributed, 
or  there  may  be  certain  regions  of  considerable  extent  which  are  quite  destitute  of 
them.  The  rhizoids  in  all  the  species  which  have  yet  been  examined  are  truly 
multicellular,  as  was  correctly  shown  by  Brebner  to  be  the  case  in  D.  simpliclfolia. 
The  nuclei  are  not  very  large,  but  can  be  readily  demonstrated. 

The  distribution  of  the  reproductive  organs  is  not  always  the  same.  Apparently 
the  usual  course  of  development  is  present  here,  the  antheridia  appearing  first  upon 
the  lower  side  of  the  midrib  and  the  adjacent  points  of  the  prothallium;  later, 
nearer  the  apex  and  upon  the  lower  side,  the  archegonia  arise.  Sometimes,  how- 
ever, as  in  the  other  forms,  there  is  a  more  or  less  marked  tendency  to  dicecism  and 
some  of  the  smaller  prothallia  seem  to  bear  only  archegonia  or  antheridia,  and  it  is 
common  to  find  antheridia   developing  exclusively  upon  the  lateral  lobes,  which 


A.  Section  of  a  >(>ung  prothallium,  showing  (\vi. 

B-E.  Longitudinal  sections  of  antheridia. 

F-H.  Transverse  sections.    G,  H  are  surface  views  showing  the  oper<  nUr  crli.    in.  iii.intlr  trlU.     \  iSo. 

I.  Cell  from  interior  of  prothallium,  showing  the  endophvte. 

apparently  never  produce  archegonia  at  all.  Antheridia  may  also  occur  upon  the 
upper  surface,  but  this  is  not  common,  and  in  no  cases  were  archegonia  seen  except 
upon  the  lower  surface  of  the  midrib.  The  reproductive  organs  are  sonutimes 
found  in  great  numbers  upon  the  older  prothallia,  the  whole  lower  surface  of  the 
midrib  being  beset  with  archegonia.  Quite  as  often,  however,  extensive  areas  along 
the  midrib  are  quite  sterile  and  the  archcgoni;i  thus  appear  in  |iatches,  sepaiattd  h\ 
sterile  intervals. 


IHK  KNDOl'HYIK  () 
rattiaceae  that  I  havt 


\I,\K  \ 


In  all  of  the  Marattiaceae  that  I  have  studied,  an  nulopln  tic  fungus  \ei\  niucli 
like  that  which  occurs  in  the  prothallium  of  the  ()phioglossace;e  has  been  found 
occupying  the  central  cells  of  the  prothallium  in  nearly  all  cases.  The  endoph\  te 
which  infests  the  green  prothallium  of  the  Marattiaceae,  when  compared  with  that 
found  in  the  strictly  saprophytic  prothallia  of  the  Ophioglossaceae,  shows  some 
differences  which  are  probably  not  without  significance.    The  structure  of  the  myce- 


128 


THE    MARATTIALES 


Hum  and  its  general  behavior  are  so  much  hke  the  form  which  occurs  in  Ophio- 
glossum  as  to  leave  little  room  for  doubt  that  the  two  forms  are  either  identical  or 
very  closely  related.  The  conidia  (fig.  g6,  /),  while  occurring  in  the  Marattiaceae, 
are  perhaps  less  frequent,  but  in  form  and  structure  are  much  like  those  of  the 
endophyte  of  Botrychnim.  The  most  noticeable  difference  is  the  absence  of  the 
digestive  cells,  i.  e.,  those  that  contain  the  varicose  swollen  mycelium.  No  evidences 
were  found  in  the  Marattiaceae  of  the  destruction  of  the  fungus  by  the  cells  of  the 
host  and  it  is  likely  that  the  endophyte  in  these  green  prothallia  is  more  nearly  a 
true  parasite  than  is  the  case  in  the  saprophytic  gametophytes  of  the  Ophio- 
glossaceae.  In  the  infested  cells  of  the  green  gametophyte  the  starch  and  chroma- 
tophores  are  destroyed  by  the  action  of  the  endophyte,  but  the  nucleus  of  the  cell 
remains  intact. 

THE  SEXUAL  ORGANS. 

THE    ANTHERIDIUM. 

The  development  of  the  antheridium,  except  for  the  details  t)f  spermatogenesis, 
was  correctly  described  by  Luerssen  and  Jonkmann  for  Marattia  and  Jngioptcn's. 
The  other  genera  agree  closely  with  these  in  the  essential  structure  of  the  antherid- 
ium. The  development  of  the  antheridium  in  the  Marattiaceae  agrees  very  closely 
indeed  with  that  of  Ophioglossuni. 


Fig.  97.— Developm 


A.  Section  of  prothallium,  bearing  antheridia  on  both  surfaces.     X8o. 

B-H.  Longitudinal  sections.     X300.    E-H,  D.  elllplica;  the  others,  D.  jamaicemis. 

The  mother  cell  of  the  antheridium,  as  in  Op/iioglossmn,  divides  first  by  a 
periclinal  wall  into  an  outer  cell,  the  primary  cover  cell,  and  an  inner  one,  from  which 
the  mass  of  spermatocytes  is  developed  (figs.  96,  97).  The  mother  cell  of  the  anther- 
idium shows  much  the  same  variation  in  form  as  that  of  Ophioglossum,  sometimes 
being  relatively  broad  and  shallow  and  at  other  times  deeper  and  narrower  (fig.  96, 
B,  C).  The  first  division  in  the  inner  cell  is  usually  transverse,  but  in  the  broader 
type  of  antheridium  this  first  wall  may  be  longitudinal.  The  primary  wall  is  followed 
by  a  second  one  at  right  angles  to  it  and  the  four  cells  thus  formed  are  again  divided 
so  that  there  result  eight  nearly  equal  cells.  The  first  wall  occasionally  is  somewhat 
oblique,  but  even  in  such  cases  the  regular  quadrant  and  octant  walls  arise  at  right 


I  III    i.AMi.iorii^i  I  12V 

angles  to  till-  |iiimai\  iluision  wall.  I  lif  ni-\r  (livisii)iis  an-,  iisuall)  at  kast,  anti- 
clinals  (fig.  97,  (7),  but  before  long  the  periclinal  walls  also  are  developed  and  sub- 
sequent divisions  do  not  show  any  recognizable  regularity  in  their  sequence;  there 
seems  to  be  a  good  deal  of  variation  in  this  respect,  even  in  the  same  species.  1  he 
number  of  cells  ultimately  formed  varies  a  good  deal,  but  the  number  of  spermato- 
cytes finally  developed  is  probably  never  so  great  as  that  found  in  some  of  the 
C)phioglossace;f.  Ktiulfitssia,  both  in  the  si/.e  of  the  antheridium  and  that  of  the 
spermatozoids,  approaches  nearest  to  Ophioglossiuti.  The  number  of  sperinat(r/.oids 
ma\  reach  several  hundred,  fifty  or  more  being  visible  in  a  single  section  of  a  large 
antheridium,  and  nearly  or  (|uite  as  many  may  sometimes  lie  found  in  Dantra, 
where,  however,  the  spermatozoitls  are  much  smaller  than  in  K (iiilfussKi. 

Ill  the  cover  cill  the  divisions  are  all  anticlinal  and  iKiri/oiual  sections  or 
surface  views  show  that  the  successive  walls  are  arranged  spiialK  in  a  way  suggesting 
the  segmentation  of  a  time-sided  apical  cell.  'i"he  last-foinud  wall  cuts  out  a  small, 
nearly  triangular  cell,  the  opercular  cell  (fig.  95  D,  E.  <>).      In  most  cases,  at  least. 


this  opercular  cell  is  thrown  off  when  the  antheridium  opens,  leaving  a  small 
aperture  through  which  the  spermatozoids  are  ejected.  Surrounding  the  mass  of 
spermatocytes  is  a  layer  of  mantle  cells  cutoff  from  the  adjacent  cells  of  the  prothal- 
lium.  These  mantle  cells,  at  the  time  of  the  opening  of  the  antheridium.  become 
very  much  distended  and  project  strongly  into  the  cavity  of  the  empty  antheridium 
(fig.  100,  /?,  til).  They  no  doubt  play  an  important  part  in  the  dehiscence  of  the  ripe 
antheridium. 

Sl'KKM  VroCENESIS.     (Plate  2,  figs  58-44.) 

()t  the  i\larattiace;e,  Kaulfiissia  is  the  most  satisfactory  for  studying  the  details 
ot  spermatogenesis,  owing  to  the  much  larger  size  of  the  spermatozoid.  The 
development  of  the  spermatozoids  agrees  very  closely  in  its  details  with  that  of 
Opiiioglossuni.  If  the  spermatocyte  is  examined  just  before  the  final  division  the 
two  blephaioplasts  can  be  seen  and  the  division  of  the  cell  into  the  two  spermatoc\tes 
proceeds  very  much  as  in  Opliioglossiini.  After  the  final  division  the  nucleus  of  the 
spermatocyte  appears  coarsely  granular  and,  as  in  other  cases,  no  nucleolus  can  be 
seen.  In  favorable  cases  the  blepharoplast  is  visible  as  a  round  body,  stained 
9 


130 


IHE    MARATTIALK! 


rather  stiongly  and  lying  near  the  nucleus.  1  he  blepharoplast  soon  takes  on  the 
curved  form  and  becomes  much  extended  and  the  cilia  begin  to  develop  from  it 
before  the  nucleus  has  materially  changed  its  shape. 

The  nucleus  now  becomes  slightly  pointed  at  one  end  and  begins  to  stretch 
out  so  as  U)  appear  somewhat  crescent-shaped,  very  much  as  in  Ophioglossuni  and 
as  it  does  in  other  ferns  that  have  been  described.  With  this  change  in  the  form  of 
the  nucleus,  the  blepharoplast  becomes  still  more  elongated  and  strongly  colored 
and  the  cilia  increase  in  length.  The  nucleus  of  the  spermatozoid  in  Kaulfiissia 
is  less  elongated  than  is  usual  in  the  ferns,  and  in  this  respect,  as  well  as  in  its  larger 
size,  it  more  nearly  resembles  Ophioglossuni  than  it  does  the  other  Marattiaceje. 
The  granular  appearance  of  the  nucleus  is  maintained  until  the  spermatozoid  is 
almost  fully  developed,  when  there  seems  to  be  a  fusion  of  the  chromosomes  so  that 
it  appears  almost  homogeneous;  this  is  accompanied  by  a  noticeable  diminution  in 
the  size  of  the  nucleus.  The  nucleus  occupies  only  the  large  posterior  coil  of  the 
spermatozoid,  while  the  anterior  portion,  which  shows  about  two  coils,  is  composed 
of  the  blepharoplast  with  probably  a  certain  amount  of  other  cytoplasmic  matter. 


Fig.  ioo. 

A.  Cross-section  of  a  ripe  anthcridium  of  D.  jamaicensii. 

B.  Cross-section  of  an  empty  antheridium ;  m,  mantle  cells. 
C-D.  Surface  views,  showing  opercular  cell. 

All  figures  X  350. 

In  Marattia  and  Angiopteris  (plate  2,  fig.  44)  the  nucleus  of  the  spermatocyte 
becomes  much  more  extended  and  the  whole  spermatozoid  is  more  slender  than  in 
Kaiilfussia.  Indeed  there  is  very  little  difference  between  the  appearance  of  the 
spermatozoids  of  Angiopteris  and  Marattia  and  those  of  the  typical  leptosporangiate 
ferns.  Some  observations  were  made  also  upon  Dancea,  in  which  the  spermatozoid 
is  somewhat  intermediate  in  character  between  that  o{  Angiopteris  and  Kaulfussta 
(plate  2,  figs.  42,  43).  In  size  the  spermatozoids  are  more  like  those  ot  Angiopteris, 
but  the  nucleus  is  much  less  elongated  and  the  general  form  of  the  spermatozoids 
is  more  like  that  of  Kaulfussia. 

THE    ARCHEGONU'M. 

The  archegonium  in  the  Marattiaceae,  like  the  antheridium,  very  much  resembles 
that  of  Ophioglossuni,  but  the  neck  of  the  archegonium  is  even  less  developed  than 
in  the  latter.  Jonkmann  (  Jonkmann  I)  has  given  a  fairly  complete  account  of  the 
development  in  Marattia  and  Angiopteris,  and  Farmer  (Farmer  1)  has  described 
and  figured  the  archegonium  of  the  latter  genus. 

Usually,  at  least,  the  archegonium  is  developed  only  upon  the  cushion  of  tissue 
back  of  the  apex,  the  young  archegonia  arising  in  acropetal  succession.    Jonkmann 


THE    t.AMI 


131 


States,  liowcvci,  that  lie  lias  tniintl  tluiii  a 
Hum,  but  noiu-  of  the  specimens  1  have 
cell  of  the  young  archegoniimi  is  scarce! 
antheiidium  and  like  it  is  first  divided  In 
and  an  inner  cell,  the  latter  usuall},  init 
central  and  a  hnsal  cell  (figs.  lOi    loj),  as 


Iso  upon  the  uppii  suit.ice  ot  the  piothal- 
ixamined  have  shown  this.  The  mothei 
V  disringuishahle  in  form  from  the  \oung 
a  jHiiclinal  wall  into  an  outer  lovei-  cell 
nor  always,  divided  suhsi(|ui  nrly  into  a 
in  O/'/iioglossinn  and  in  the  t\  jiical  ferns. 
Sometimes  the  mothei  cell  of  the  archegonium  is  seen  in  tians\erse  section  to  have 
been  cut  out  veiy  nuich  as  the  axial  low  of  cells  arises  in  the  archegonium  of  the 
Hepaticiv.  Ihere  seems  no  question  that  the  so-called  mother  cill  of  the  archego- 
nium in  all  the  ferns  is  really  homologous  onl\   \\uh  rhi    axial   vow  of  cells  of  rhi- 


'fi 


rthe 


opm 


br\-ophyte  archegonium,  the  four  rows  of  neck  cell 
of  the  terminal  cap  cell  of  the  liverwort  archegoniu 

The  inner  of  the  two  primary  cells,  as  we  have  alreach  statid,  ma\  havi'  a  basal 
cell  cut  off  from  it  before  the  further  divisions  arise,  by  which  the  egg  cell  and  the 
canal  cells  are  divided.  I'he  neck  canal  cell  is  very  broad  and  may  become  divided 
into  two  cells,  but  usually  the  division  is  confined  to  the  nucleus,  which  probabi)' 
divides  in  all  cases.  1  he  ventral  canal  cell  cut  off  in  the  usual  fashion  from  the  egg 
is,  with  the  exception  of  Datura,  very  large  and  conspicuous,  thus  differing  from 


\Tc\\r^on\A  o{  Angiofiterii.     X275.    6,  ba 


Ophioglossum,  where  the  ventral  canal  cell  is  so  difficult  to  demonstrate;  bur  in 
Datura  there  is  the  same  imperfect  development  ot  the  ventral  canal  cell  that  is 
found  in  Ophioglossutri. 

As  the  archegonium  approaches  maturity  a  layer  ot  mantle  cells,  much  like 
those  which  surround  the  antheridium,  is  cut  off  from  the  tissue  surrounding  the 
venter  of  the  archegonium.  The  archegonia  of  Marattia  douglasii  are  confined  to 
the  lower  side  of  the  midrib  and  begin  to  form  at  some  distance  back  of  the  grow- 
ing point;  so  tar  as  can  be  determined,  any  superficial  cell  of  the  apical  meristem 
can  develop  into  an  archegonium.  The  mother  cell  divides,  as  we  have  seen, 
into  three  superimposed  cells,  of  which  the  lowest,  /;,  usually  divides  later  by 
vertical  walls,  and  forms  the  base  of  the  archegonium.  From  the  central  one,  b\- 
transverse  divisions,  are  formed  the  canal  cells  and  egg,  and  from  the  uppermost 
the  neck.  Compared  with  the  typical  ferns,  the  most  striking  differences  are  the 
short  neck  and  the  very  broad  canal  cells.  The  cover  cell  undergoes  division  into 
four,  by  two  intersecting  vertical  walls,  as  in  Ophioglossutri,  and  each  of  these  four 
cells  then  undergoes  division  by  nearly  horizontal  walls,  but  the  cells  remain  short, 
so  that  the  neck  projects  very  little  and  there  are  only  three  or  four  cells  in  each  row; 
occasionally  there  may  be  only  two.  Jonkmann  states  that,  as  a  rule,  two  of  the 
rows  of  the  neck  contain  three  cells  and  two  contain  tour,  but  that  there  may  occa- 
sionally be  as  many  as  five.  The  neck  canal  cell  often  shows  a  trace  of  a  division  and 
there  ma\-  he  an  :ictual  division  w:ill  t'ormed  (fig.  loi,  D),  hut  in  Marattia  douglasii 


132 


THK    MARATTIALES 


this  is  not  ordinarily  the  case.  In  one  instance  in  this  species  I  observed  a  division  by 
a  vertical  wall,  so  that  two  neck  canal  cells  were  formed,  placed  side  by  side,  in  a  way 
recalling  very  strongly  the  division  of  the  neck  canal  cell  described  by  Jeffrey  in 
certain  species  of  Equisetnm  (Jeffrey  2).  The  central  cell  is  divided  again  by  a  hori- 
zontal wall  into  two  nearly  equal  cells,  the  lower  one  being  the  egg,  the  upper  one  the 
ventral  canal  cell.  The  mature  egg  is  nearly  elliptical  in  form,  the  upper  third  being 
almost  homogeneous  and  quite  colorless,  forming  the  so-called  receptive  spot.  The 
nucleus  is  of  moderate  size  and  does  not  stain  very  strongly.  The  archegonium  of 
Augiopteris  closely  resembles  that  of  Marattia,  but  is  perhaps  somewhat  narrower 
(fig-  loi). 

Jonkmann  figures  the  archegonium  ot  M.  ficittafolia,  which  shows  that  this 
species  also  is,  in  the  relative  size  of  the  canal  and  neck  cells,  very  much  like  Angi- 
opteris.  Farmer  thought  that  a  basal  cell  was  usually,  if  not  always,  present,  and  my 
own  studies  tend  to  confirm  this. 


Archegonia  of  Kmill 


,  neck  canal  cell. 


In  Kaulfussia  (fig.  102)  the  archegonia  form,  as  a  rule,  only  after  the  antheridia 
have  ceased  to  develop.  Compared  with  the  other  Marattiaceae  they  are  decidedly 
large,  and  in  this  respect  Kaulfussia  approaches  Ophioglossum.  Like  the  mother 
cell  of  the  antheridium,  there  is  a  good  deal  of  variation  in  the  width  of  the  young 
archegonium  in  Kaulfussia.  Some  of  the  narrower  types  recall  the  archegonium 
of  Anthoceros  and  emphasize  the  resemblances  between  the  archegonium  of  the 
Anthocerotaceae  and  the  eusporangiate  ferns.  The  neck  of  the  archegonium  is  very 
short,  each  of  the  four  original  neck  cells  often  dividing  only  once,  so  that  there  may 
be  but  two  cells  to  each  of  the  four  rows.     More  commonly,  however,  there  is  a 


second  division  in  some  of  the  cells,  so  that  each  row  consists  of  three  cells.  The 
nucleus  of  the  broad  neck  canal  cell  probably  always  divides,  but  the  number  of 
available  specimens  was  too  small  to  decide  whether  or  not  there  is  ever  formed  a 
division  wall  between  these,  although  it  is  not  at  all  unlikely  that  this  may  occur. 
The  ventral  canal  cell  is  conspicuous  and  equals  its  sister  cell,  the  egg,  in  breadth. 
In  the  peripheral  portion  of  all  the  axial  cells  of  the  archegonium  there  are  many 
small  granules  of  starch.  Jonkmann  figures  similar  starch  granules  in  both  Marattia 
and  Angiopteris. 


THE    GAMETOPHYTE 


133 


Ihe  archegonium  in  Danaa,  while  resembling  that  of  the  other  Marattiaceae, 
in  its  position  and  early  development  shows  some  marked  differences,  the  signifi- 
cance of  which  is  not  quite  clear.  The  division  of  the  mother  cell  into  the  primary 
neck  cell  and  the  central  cell  follows  in  the  same  way  as  in  the  other  forms,  but  the 
inner  cell,  usually  at  least,  does  not  have  a  basal  cell  separated  from  it,  but  develops 
at  once  into  the  egg  cell  and  canal  cells.  The  absence  of  the  basal  cell  is  by  no  means 
unknown,  however,  among  the  other  Marattiaceic.  The  primary  neck  cell  gives 
rise  to  the  usual  four  cells,  each  of  which  divides  into  three  or  four,  and  exception- 
ally into  five.  There  is  a  marked  elongation  of  the  inner  cell  before  its  separation 
into  the  central  cell  and  the  neck  canal  cell  (fig.  103,  D). 


Up  to  this  point  there  is  nothing  peculiar  in  the  development  of  the  archegonium 
in  Danaa,  but  while  in  most  of  the  other  Marattiaceae  a  conspicuous  ventral  canal 
cell  is  formed,  its  sister  cell  being  the  egg,  in  Datura  the  formation  of  a  definite 
ventral  canal  cell  couKl  nor  be  satisfactorily  demonstrated.  In  a  number  of  cases 
(fig.    10^;  phue  i,  fio.  4S)  ;i   siikiII  nucleu.s-like  body  could   be  seen  in  a  large,  clear 


space  just  above  the  somewhat  contracted  mass  of  protoplasm,  with  its  laiue  and 
conspicuous  nucleus,  which  constitutes  the  egg  cell;  but  this  ventral  canal  cell 
nucleus,  if  such  it  is,  is  very  different  in  appearance  from  the  large  and  conspicuous 
one  found  in  the  other  Marattiaceae,  and  in  the  absence  of  anv  division  stages  its 
nuclear  nature  must  for  the  present  remain  somewhat  doubtful. 

There  is  somewhat  the  same  uncertainty  in  regard  to  the  primary  division  of  the 
neck  canal  cell.  This  possesses  a  large  and  conspicuous  nucleus  which  in  large  and 
apparently  mature  archegonia  was  still  undivided.  In  a  few  cases  a  division  of  the 
protoplasm  in  the  neck  cells  was  observed;  in  other  cases,  without  any  such  division. 


134  THE    MARATTIAI.KS 

a  second  body  ot  rather  indefinite  outline  and  staining  much  less  strongly  than  the 
lower  nucleus  could  be  made  out;  but  up  to  the  present  time  I  have  not  been  able 
to  satisfy  myself  that  the  division  of  the  neck  canal  cell  nucleus,  which  always 
occurs  in  the  other  Marattiaceae,  takes  place  here.  The  very  uncertain  nature  of  the 
ventral  canal  cell  recalls  strongly  the  condition  of  affairs  in  Ophioglossum,  where  it 
is  equally  difficult  to  demonstrate  satisfactorily  the  presence  of  a  true  ventral  canal 
cell. 

FERTILIZ.^TION. 

It  has  not  been  possible  to  follow  in  detail  the  process  of  fertilization  in  the 
Marattiaceae,  but  several  stages  were  found  in  preparations  of  Marattta  douglasii. 
The  entrance  of  the  spermatozoid  into  the  archegonium  was  not  seen,  but  in  a 
number  of  cases  the  material  had  been  killed  immediately  after,  and  twice  spermato- 
zoids  were  found  which  had  penetrated  into  the  egg.  In  these  cases  the  spermato- 
zoid was  quite  unchanged  in  form,  but  had  not  yet  entered  the  nucleus  itself.  One 
case  was  observed  where  there  were  apparently  two  nuclei  in  close  contact,  but  the 
egg  nucleus  was  much  contracted  and  it  is  doubtful  whether  this  was  really  a  normal 
appearance.  It  is  probable  that  the  details  of  fertilization  are  quite  similar  to  those 
observed  in  other  ferns. 


135 


11.    rilK    LMHRYO. 


The  study  of  the  embryogeny  of  the  Marattiaceae  offers  many  difficulties. 
Fertilization  does  not  seem  to  be  of  common  occurrence  and  a  very  large  number  of 
prothallia  must  be  examined  before  even  a  small  series  of  embryos  can  be  secured; 
moreover,  the  earlier  stages  of  the  embryo  are  peculiarly  liable  to  shrinkage  in 
preparing  them  for  sectioning  and  it  is  exceedingly  difficult  to  secure  really  satis- 
factory preparations  of  these  early  stages. 

A  marked  peculiarity  of  the  young  sporophyte,  which  was  first  shown  by  Luers- 
sen  and  Jonkmann  for  Marattia  and  Aiigiopteris,  is  the  orientaticjn  of  the  primary 
organs  of  the  young  sporophyte  with  reference  to  the  archegonium.  The  primary 
or  basal  wall  in  the  embryo  is  always  transverse,  as  it  usually  is  in  Ophioglossum, 
instead  of  being  vertical  as  in  most  of  the  typical  ferns.  The  first  leaf,  instead  of 
being  formed  from  the  portion  of  the  embryo  nearest  the  archegonium,  as  it  is  in 
the  common  ferns,  arises  from  the  half  of  the  embryo  which  is  turned  awa\'  from  the 
archegonium,  and  grows  straight  upward,  bursting  through  the  prothallium  u|)on 
its  upper  surface,  instead  of  appearing  upon  the  lower  side  of  the  prothallium  and 
curving  upward.      Ihe  external  organs  of  the  young  sporophyte  are  dificrentiated 


A.  Two  iongitudii 

B.  A  similar  sectif 

C.  Three  transver 


1  sections  of  a  young  embryo,    t  i,  basal  wall.     X200. 

of  an  older  embryo,    cor,  cotyledori;  r,  root  initial. 

sections  of  a  much  older  embryo,  showing  junction  of  the  two  first 


much  later  than  is  the  case  in  the  Leptosporangiates,  and  the  Marattiaceae  in  this 
respect  closely  approach  the  Ophioglossaceae. 

It  has  been  generally  assumed  that,  as  in  the  leptosporangiate  ferns,  the  cotyle- 
don and  stem  are  of  epibasal  origin,  the  root  and  foot  hypobasal.  This  conclusion 
was  reached  by  both  Jonkmann  and  Farmer,  and  my  early  studies  on  Marattia 
douglasii  led  me  to  the  same  conclusion.  A  further  study  of  this  species,  however, 
as  well  as  an  examination  of  the  embryos  of  Angiopteris,  Kaidftissia,  and  Datura, 
has  shown  that  this  is  not  the  case,  but  that  the  whole  of  the  hypobasal  region  is 
devoted  to  the  formation  of  the  foot,  and  the  root  is  developed  secondarily  from  the 
epibasal  region,  from  which  are  also  derived  the  stem  apex  and  the  cotyledon. 

While  in  the  typical  ferns  the  young  organs  of  the  embryo  at  a  very  early  stage 
show  a  definite  apical  growth,  the  apical  cells  being  readily  traceable  to  the  primary- 
octants  of  the  embryo,  this  is  by  no  means  so  readily  shown  in  the  Marattiace;e. 
In  the  later  stages,  such  initial  cells  can  be  seen  in  the  root  and  stem  at  least,  but  the 
relation  of  thesi'  initial  ceils  of  rhe  root  and  stem  to  the  earl\-  tli\isions  of  the  embr\() 
is  ver\-  difficult   to  (len-rminc      In    M.dniiclasn    (Caniiihell   .? )    I    .tatiti   rhat   there 


136  THE    MARATTIALES 

was  probably  a  single  initial  in  the  stem  and  in  the  primary  root,  and  Farmer  also 
thought  that  a  single  root  initial  was  always  present  in  Angiopterts,  but  concluded 
that  such  an  initial  cell  was  not  present  in  the  stem  of  the  young  sporophyte.  Breb- 
ner  (Brebner  2)  says  that  in  Dancea  simplictfolia  such  a  single  initial  cell  seemed 
to  be  always  present  in  the  stem,  and  my  studies  on  Angiopteris,  Kaiilfussia,  and 
Dancsa  indicate  that  a  single  initial  is  developed  at  an  early  period  in  the  stem  apex 
and  persists  until  the  sporophyte  has  developed  several  leaves. 

Before  any  division  occurs  in  the  embryo  the  fertilized  cell  increases  markedh 
in  size,  after  which  there  is  formed  the  horizontal  basal  wall  (figs.  io6,  109,  Ij  b). 
This  is  probably  followed  at  once  by  the  median  wall  (except  in  Dancea),  so  that  the 
embryo  at  this  stage  is  divided  into  four  approximately  equal  quadrants  (see  Jonk- 
mann  3,  fig.  9). 

The  genus  Daiicea,  at  least  this  is  true  for  D.  jamaiceiisis  and  D.  eUiptica, 
differs  in  the  early  divisions  of  the  embryo  from  the  other  Marattiaceae.  The  egg 
cell  after  fertilization  elongates  in  a  way  which  closely  resembles  that  found  in 
Botrychium  ohUquum  (Lyon  1).  The  primary  hypobasal  cell  either  divides  no  further 
or  only  once  and  forms  a  short  suspensor,  so  that  all  the  organs  of  the  young  embryo, 
including  the  foot,  are  really  of  epibasal  origin.  As  \'et  no  trace  of  such  a  suspensor 
has  been  found  in  the  other  Marattiaceae. 

THE  EMBRYO  OE  MARATTLA. 

Luerssen  (Luerssen  2)  found  the  one-celled  embryo  and  young  plants  of 
Marattia  cirutwfoUa,  but  was  not  able  to  procure  the  older  embryos.  The  writer 
(Campbell  3)  succeeded  in  procuring  several  stages  of  the  embryo  in  Murtittia 
douglasii,  and  somewhat  later  Luerssen  described  and  figured  some  of  the  earlier 
stages  in  M.  fraxinea  and  M.  wettimantiKrfolia.  These,  so  far  as  1  am  aware, 
complete  the  list  of  records  upon  the  embryo  o{  Marattia. 

The  fertilized  ovum  in  Marattia  doHglasii  becomes  much  enlarged  before  it 
divides  and  completely  fills  the  venter  of  the  archegonium.  The  granular  contents 
of  the  egg  cell  become  evenly  distributed  without  any  apparent  increase  in  quantity 
as  the  fertilized  ovum  grows,  so  that  the  one-cell  embryo  contains  comparativel\- 
little  granular  contents,  but  the  nucleus  is  very  conspicuous.  At  the  time  of  the 
first  division  the  young  embryo  is  almost  perfectly  globular  in  form.  I  was  unable 
to  find  the  stages  immediately  following  this,  but  jonkmann  has  figured  an  eight- 
cell  embryo  of  M.  fraxinea  (see  Jonkmann  3,  fig.  9).  The  basal  wall  is  transverse 
and  this  is  followed  successively  by  the  median  and  transverse  walls,  so  that  the 
globular  embryo  is  divided  into  approximately  equal  octants.  From  the  hypobasal 
half,  which  is  nearest  the  archegonium,  there  is  developed  the  foot  alone,  while  all 
of  the  other  organs  arise  from  the  epibasal  portion,  which  is  turned  away  from  the 
archegonium. 

The  youngest  embryo  (except  the  one-celled  stage)  which  I  found  in  M. 
douglasii,  is  shown  in  fig.  106,  A.  This  is  about  the  same  stage  as  the  one  shown  in 
Jonkmann's  figs.  11  and  13.  Unfortunately  this  embryo  was  rather  badly  shrunken 
in  the  process  of  embedding  and  the  division  walls  were  a  good  deal  distorted,  so 
that  it  is  rather  hard  to  determine  exactly  their  correct  relation  to  each  other;  but 
probably  the  wall  h  h  represents  the  basal  wall  and  m  the  median  wall.  The 
embryo  has  now  lost  its  original  globular  form  and  become  oval,  the  long  axis  lying 
transversely.  The  secondary  divisions  in  the  octants  are  mostly  anticlinals,  and  the 
first  periclinals  have  just  appeared  in  a  few  of  the  cells.  Figure  106,  A,  shows  two 
consecutive  median  sections.  It  will  be  seen  that  cell  division  is  more  active  in  the 
epibasal  portion  than  in  the  hypobasal  region. 


PHI 


•MI1K'|( 


13: 


In  my  original  snid\-  <>{' Murattni  I  t'dncliidtd  that  the-  primary  divisions  n-sulted 
in  the  estabhshmcnt  of  the  organs  of  the  voiing  sporophyte  in  a  manner  similar  to 
that  in  the  l>ept()sporangiat:c,  i.  e.,  that  the  stem  and  leaf  were  derived  from  the 
epibasal  (]nadrant,  the  root  and  foot  from  the  hypobasal  ones.  Farmer  thought  that 
this  was  true  for  Angiopteris  and  Jonkmann  assumes  that  it  is  the  case  also  in 
Marattia.  A  fuither  study  of  my  preparations,  however,  has  led  me  to  believe  that 
the  whole  of  the  hypobasal  region  is  devoted  to  the  foot,  while  the  root,  together  with 
the  leaf  and  stem  apex,  are  of  epibasal  origin.  A  large  cell  (hg  \ob,A)  occupies 
approximately  the  same  position  as  the  stem  apex  in  the  older  embryo  and  it  is 
possible  that  this  may  be  the  apical  cell  of  the  stem,  but  in  the  absence  of  the  inter- 
mediate stages  this  can  not  be  positively  asserted.  For  a  long  time  the  embryo 
retains  the  oval  form  and  there  is  scarcely  any  sign  of  the  young  organs  of  the 
sporophyte  which  in  the  leptosporangiate  ferns  are  so  early  manifest;  indeed, 
Jonkmann  states  that  there  is  no  differentiation  at  all,  but  a  careful  study  of  the 
older  embryo  shows  unmistakable  indications  of  the  definitive  organs.  The  devel- 
opment of  the  tissue  in  the  epibasal  region  is  not  uniform,  but  somewhat  to  one 
side  of  the  center  (fig.  io6,  B)  there  may  be  seen  a  group  of  columnar  superficial 
cells,  which  mark  the  position  of  the  future  growing  point  of  the  stem.  Wlurher 
one  of  these  supeificial  cells  is  the 
definitive  apical  cell  it  is  impossible 
to  determine,  but  from  a  compari.son 
with  the  older  stages,  as  well  as  with 
)rresponding  stages  of  the  embryo     ) 


in  the  oti 

hi  ■,  at    least,   tha 

and  perhajis  this 

traceil  back  to  tl 

cell  noted  in  the  \()imt£e 


genera. 


t  seems  pro 

this  is   the  c; 

nitial  cell  ma\ 

centralh'  pla 

v<). 


ba- 


in b 


considerable  portion  of  the  epibasal 
tissue  is  not  uicUuleil  ui  the  men- 
stematic  region,  winch  is  tleiued 
mainly,  at  least,  from  only  one  of  the 
original  epibasal  quadrants.  The 
tissue  adjacent  to  this  meristematic  region  is  made  up  of  large  cells  with  less  dense 
contents  and  smaller  nuclei  and  differs  in  no  way  from  the  large  cells  of  the  foot,  into 
which  this  tissue  insensibly  merges  and  of  which  it  may  be  said  to  constitute  a  part. 
In  the  embryo  figured,  it  was  not  quite  certain  whether  the  root  apex  had 
begun  to  form  or  not.  It  seems  probable  that  the  cell  r  is  really  the  apical  cell 
of  the  young  root,  but  except  for  its  position  it  was  not  noticeably  different  from  the 
cells  adjacent;  however,  as  in  Angiopteris  and  Datura  there  is  no  question  that  the 
root  originates  in  this  position,  it  is  probable  that  this  cell  is  really  the  initial  for  the 
young  root  and  is  cut  out  from  the  base  of  the  epibasal  tissue  near  its  junction  with 
the  foot.  This  marked  endogenous  formation  of  the  root  is  very  much  like  that  in 
the  embryo  of  Opliiogloisiini  nioliiicauiini,  but  differs  entirely  fVom  the  superficial 
origin  of  the  apical  cell  of  the  root  in  the  embryo  of  the  Leptosporangiates. 

The  stem  apex  in  the  older  emhr\(>  is  of  very  limited  extent,  consisting  of  onl\- 
a  few  cells,  of  which  one,  as  we  have  said,  is  probably  the  definite  apical  cell,  although 
it  must  be  said  that  this  point  is  very  difficult  to  decide,  as  all  of  the  central  cells 
of  this  apical  group  look  a  good  deal  alike,  but  a  careful  study  of  both  transverse 
and  longitudinal  sections  seems  to  point  to  one  of  these  as  the  apical  cell,  which  in 
shape  is  a  good  deal  like  that  in  the  stem  apex  of  Ophioglossum.     In  longitudinal 


138 


THE    MARATTIALE5 


sections  this  is  somewhat  wedge-shaped,  the  narrow  end  turned  outward  and  the 
broad  base  below.  In  cross-section  this  cell  is  nearly  square  in  shape  (fig.  107,  A,  x) 
and  there  may  be  seen  a  fairly  regular  series  of  four  segments  cut  from  the  lateral 
faces.  From  the  broad  truncate  base  of  the  cell,  segments  are  also  cut  off  which 
contribute  to  the  inner  tissue  of  the  stem.* 

Much  the  greater  part  of  the  epibasal  meristem  contributes  to  the  cotyledon, 
which  is  soon  evident  as  a  broadly  conical  protuberance,  somewhat  flattened  on  the 
side  adjacent  to  the  stem  apex  and  merging  gradually  on  the  outer  side  into  the  large- 
celled  tissue  which  adjoins  the  foot.  To  judge  from  the  limited  number  of  young 
embryos  which  I  could  examine,  it  seems  that  the  growth  of  the  cotyledon  is  not  due 
to  the  activity  of  a  single  apical  cell,  but  this  point  was  somewhat  uncertain. 

By  the  time  that  the  cotyledon  is  established,  growth  has  progressed  in  the  young 
root,  which  now  is  seen  to  have  a  conspicuous  apical  cell,  which  divides  rapidly 
so  that  the  root  quickly  elongates  in  a  direction  opposite  to  that  of  the  cotyledon 
(fig.  108).  The  apical  cell  of  the  primary  root  in  M.  douglasii  is  not  triangular  in 
outline,  but  more  or  less  quadrilateral,  whether  seen  in  longitudinal  or  cross 
sections  (fig.  107,  B).  In  form  and  segmentation  it  perhaps  more  nearly  resembles 
that  of  Daiura  than  it  does  the  tetrahedral  apical  cell  which  occurs  in   the  young 

primary  root  oi Angwpteris. 
Active  cell  divisions  take 
place  also  in  the  tissue  of 
the  foot,  which  completely 
incloses  the  young  root  and 
becomes  practically  merged 
with  it,  so  that  it  is  quite 
impossible  to  say,  at  the  time 
the  root  emerges,  just  how 
much  of  the  tissue  ot  its 
outer  portion  really  belongs 
to  the  root  itself  and  how 
much  is  derived  from  the 
original  tissue  of  the  foot. 
The  latter  is  now  no  longer 
recognizable  as  such,  the 
young  sporophyte  apparently  at  this  time  being  composed  almost  entirely  of  the 
cotyledon  and  the  very  large  root,  with  the  stem  apex,  lying  near  their  junction. 
From  a  comparison  with  younger  stages,  however,  it  is  perfectly  evident  that  the 
enlarged  central  region  of  the  embryo  at  this  time  is  composed  mainly  of  tissue 
belonging  to  the  foot,  which  is,  so  to  speak,  perforated  by  the  root  in  its  downward 
growth. 

The  development  of  the  vascular  bundles  at  a  very  early  period  is  first  evident 
in  the  cotyledon,  which  almost  as  soon  as  it  can  be  recognized  at  all  is  seen  to  have 
a  strand  of  procambium  extending  below  it.  If  this  procambium  strand  is  traced 
downward,  it  is  seen  to  continue  without  interruption  into  the  base  of  the  root,  exactly 
as  it  does  in  Ophtoghssum  moluccanum.  No  trace  of  a  procambial  cylinder  can  be 
found  extending  into  the  stem  apex,  which  gives  rise  only  to  the  parenchyma  of  the 
central  pith.  This  early  development  of  the  vascular  bundles  in  the  cotyledon  and 
root  was  correctly  observed  by  Jonkmann  and  Farmer,  both  for  Marattia  and 


A.  Section  of  an  advanced 

emergence  of  cotyled 

B.  The  cotvledon,  more  er 


*  In  a  very  recent  paper 
tem  in  Marattia  alata  is  at  first 
group  of  initial  cells. 


l),  Miss  Charles   states   tha 
r  sporophvtes  the  single  api( 


the  apical  cell  of  the 
I  cell  was  replaced  by 


THE    EMBRYO 


139 


Angiopteris,  but  they  seem  to  rakr  it  for  granted  that  a  vascular  strand  is  also 
developed  in  the  stem;  at  any  rate  the\-  make  no  reference  to  the  absence  of  such 
a  vascular  strand  from  the  stem  region.  In  my  earlier  study  of  Marattia,  I  supposed 
that  a  strand  was  developed  which  belonged  to  the  stem  itself,  but  a  further  exam- 
ination of  many  plants,  after  a  study  of  this  point  in  the  other  genera,  has  made  it 
pretty  clear  that  this  supposed  stem  bundle  really  belongs  to  the  second  leaf,  the 
rudiment  of  which  appears  at  a  very  early  period. 

rilK  KMHRYO  OF  ANCIOI'TI- RIS. 

In  Angiopteris  the  embryo  very  early  becomes  more  greatly  elongated  trans- 
versely than  is  the  case  in  Marattia,  so  that  in  a  longitudinal  section  it  appears  as  a 
very  much  depressed  oval  (fig.  109);  the  cpibasal  region  is  larger  than  the  hypobasal 


A.  Two  sections  of  a  young  embryo  of  Angiopteris. 

B.  Diagrams  showing  arrangement  of  cells  of  same 

C.  An  oljer  embryo,    b  h,  basal  wall;   si,  stem  apex 


and  the  quadrant  divisions  are  often  still  evident.  Whether  octant  divisions  are 
formed  in  all  the  quadrants  could  not  positively  be  determined,  but  Jonkmann 
states  that  such  is  the  case.  There  can  usually  be  found  in  the  young  embryo  a 
nearly  centrally  placed  large  cell  (fig.  109,  C.  st),  which  probably  is  the  initial  cell  of 
the  young  stem.     The  position  of  this  cell  is  not  unlike  that  which  occurs  in  the 


nhryooi  Angiopteris.    X200.    The  yovmg  root, 
:x;  col,  cotyledon;  /,  foot. 


embryo  of  Eqtiisettini,  and  at  this  stage  there  is  also  a  certain  resemblance  to  the  em- 
bryo of  Botr\chium  virginuinum.  As  the  embryo  grows  it  tends  to  assume  a  more 
nearly  globular  form  (fig.  i  lo).  The  basal  wall  can  still  be  imperfectly  followed,  the 
hypobasal  portion  of  the  embryo  being  made  up  of  the  large  cells  forming  the  foot, 
while  above  the  basal  wall  the  cell  divisions  are  more  active  and  the  rudiments  of 


140 


THE    MARATTIALES 


the  Stem  and  cotyledon  can  be  recognized,  although  the  embryo  still  retains  its  oval 
outline.  As  in  the  embryo  of  Marattia,  growth  is  most  active  in  the  central  region 
of  the  epibasal  part  of  the  embryo  and  there  can  generally  be  recognized  a  large 
central  cell,  which  is  presumably  the  single  initial  of  the  stem  apex,  although,  as 
in  the  case  oi  Marattia,  it  is  not  absolutely  certain  that  a  single  initial  cell  is  always 
present.  Cell  division  is  especially  active  on  one  side  of  the  stem  apex,  and  this 
area  marks  the  position  of  the  young  cotyledon.    The  limits  of  this  growth  area 


A.  Two  longitudinal  sections  of 

B.  Stem  region  of  same  embryo.     Xi6o. 

C.  Root  apex.      Xl6o. 

not  very  sharply  defined  and  it  is  difficult  to  say  whether  it  can  be  traced  back  to 
a  single  quadrant  or  octant  cell,  but  it  is  probably  not  always  constant  in  its 
position;  indeed,  the  stem  looks  as  if  the  stem  apex  and  the  cotyledon  both  arose 
from  the  same  quadrant,  the  second  epibasal  quadrant  contributing,  at  least  in 
part,  to  the  foot. 

As  seems  to  be  true  in  all  the  Marattiaceae,  the  root  makes  its  appearance  at  a 
comparatively  late  period  and  it  is  evident  that  the  root,  as  in  the  embryo  of  Maratlia, 
is  a  strictly  endogenous  structure.    The  first  indication  of  the  root  is  the  development 


A.  Longitudinal  section  of  an  advanced  embryo  of  An 

B.  Cotyledon  of  same  embryo,  showing  dichotomy  of 

C.  Root  apex  of  same.     X220. 


of  the  cotyledon.    X50. 


of  a  group  of  actively  dividing  cells,  almost  in  the  center  of  the  embryo  below  the 
stem  apex.  This  meristematic  region  is  probably  always  of  epibasal  origin,  but  it  is 
close  to  the  basal  wall  and  it  is  possible  that  sometimes  it  may  arise  below  it.  The 
apical  cell,  which  in  the  early  stages  almost  always  appears  triangular  in  section, 
becomes  conspicuous  and  was  recognized  by  Farmer  in  his  study  of  the  embryo  of 


Tin:     IMI'.R'iO  141 

Jiigioptcns  {Fainifi  I).  Tin-  loor  initial  now  divitlcs  by  icj^Lilar  SLiinicntatidn  and 
the  root  apex  pushes  rapidly  down  tlirough  the  underlying  toot  and  ultimately 
emerges  on  the  lower  side  of  the  prothallium.  In  the  meantime  the  cotyledon  grows 
actively  and  there  is  a  rapid  elongation  of  the  whole  embryo  in  a  vertical  direction. 
As  in  the  case  of  Mcirattia,  it  is  difficult  to  prove  that  the  cotyledon  grows  from  a 
single  initial  cell.  The  cotyledon  has  very  much  the  form  of  that  in  Marattia, 
growth  being  more  active  on  the  outer  side,  so  that  it  curves  over  the  stem  ape.x 
very  much  as  the  cotyledon  does  in  the  embryo  of  Hotrycliiiini  virgiiiiatium.  About 
the  time  that  the  cotyledon  is  ready  to  emerge,  the  apex  becomes  flattened  out  and 
(sometimes,  at  any  rate)  there  is  a  true  dichotomy  of  this  apex  (see  fig.  112,  B). 

In  the  primary  root  there  seems  to  be  no  question  of  the  presence  of  the  single 
initial  cell  which,  at  first  at  least,  has  the  tetrahedral  form,  but  later  on  is  apt  to 
have  the  base  truncate,  although  it  usually  has  three  series  of  lateral  segments. 
I  have  not  been  able  to  confirm  Farmer's  statements  that  the  single  apical  cell  is 
later  replaced  by  a  group  of  similar  initials,  as  in  the  later  roots  of  the  sporophyte, 
although  it  is  not  at  all  impossible  that  such  may  sometimes  be  the  case.  The 
development  of  the  embryo  of  the  vascular  bundles  in  the  young  sporophyte  is 
exactly  the  same  as  in  the  coiiesponding  stages  of  the  embrvo  ni  Mmattin. 


rilK   KMIUnO  ()1-    KAUI.I  TSSIA. 

So  far  as  I  am  aware,  no  account  has  been  published  of  the  embijo  ui  kuul- 
fiissiii,  except  one  of  my  own  (Campbell  II).  Only  two  young  embryos  were  found, 
so  that  it  was  impossible  to  follow  in  detail  the  early  history  of  the  young  sporophyte. 
The  basal  wall,  as  in  the  other  Marattiaceae,  is  transverse  and,  to  judge  from  a 
comparison  of  similar  stages  of  the  embryo  in  Marattia  and  Aiigiopten's,  all  of  the 
organs  of  the  young  sporophyte  in  Kaulfussia,  except  the  foot,  are  also  of  epibasal 
origin.  Figure  113,  A,  shows  a  nearly  median  longitudinal  section  of  the  young 
embryo.  This  is  very  much  elongated  transversely,  and  to  judge  from  the  position 
of  the  cells  the  basal  wall  is  probably  followed  by  the  median  walls,  forming  nearly 
equal  quadrants.  The  large  cell  {st)  in  one  of  the  epibasal  quadrants  corresponds 
in  position  to  the  similar  cell  found  in  the  embryos  of  the  other  genera  and  very 
likely  may  represent  the  primary  initial  cell  of  the  stem.     The  embryos,  however. 


Fig.  1 13.— Young  embryos  of  Kimljuniit.     X275. 

a  similar  embryo,    hh,  ba^al  wall;    n,  t]iiadrant  wall. 

were  too  young  to  make  clear  the  relation  of  the  cotyledon  and  primary  root  to  the 
stem.  Three  nearly  transverse  sections  of  an  embryo  of  about  the  same  age  are 
shown  in  fig.  113,  B.  To  judge  from  the  structure  of  the  older  sporophyte  at  the 
time  when  it  first  emerges  from  the  prothallium,  Kaulfussia  agrees  in  the  main  with 
Marattia  and  Angiopteris  in  the  origin  of  the  young  organs  of  the  sporophAte. 


142 


THE    MARATTIALE; 


THE  EMBRYO  OF  DAN.+'.A. 

liiebiKT  (Brebnci  2)  has  described  the  older  enibiyt)  of  Duiura  simpliiifolm, 
but  did  not  secure  the  earlier  stages.  The  youngest  specimens  he  figures  closely 
resemble  in  form  a  corresponding  stage  in  the  species  studied  by  me,  and  the  slightly 
pointed  basal  region  suggests  the  possibility  of  the  presence  of  a  short  suspensor 
in  D.  simpUcifolia  like  that  which  I  have  found  in  D.  jamaicensis  and  D.  elliptua. 
While  my  own  collection  of  young  embryos  is  not  as  complete  as  might  be  wished, 
still  enough  stages  were  secured  to  show  that  at  least  D.  jamaiceusis  and  D.  rlli pticu 


A.  Archegoniuni  containing  a  one-celled  embryo 

B.  Outline  of  next  section  of  same  embryo. 

C.  Three-celled  embryo,  showing  suspensor,  ius. 

D.  Outline  of  next  section  of  the  same  embryo. 


E.  Three  longitudinal  sections  of  a  four-celled 

F.  .An  older  embryo,  which  was  shrunken. 

G.  Diagram  of  F,  showing  probable  arrangen 


nbryo. 
It  of  cells. 


differ  remarkably  from  the  other  Marattiacea?  that  have  been  studied  in  the  develop- 
ment of  a  short  suspensor,  thus  showing  an  interesting  analogy  with  the  embryo  of 
Botrychium  obliquum,  described  by  Lyon  (Lyon  1).  Whether  D.  jenmani  shows 
the  same  peculiarity  was  not  determined,  on  account  of  the  failure  to  obtain  the 
young  embryo  of  this  species;  but  as  in  its  later  development  it  corresponds  very 
closely  to  the  other  species,  it  is  highly  probable  that  a  suspensor  is  developed. 


section  of  an  older  embryo  of  D.  jamaicensis.    The  su 
B.  Three  sections  of  a  young  embryo  of  D.  elliptica.     sus,  suspensor.      X200. 

Before  the  first  division  takes  place  in  the  embryo,  the  fertilized  ovum  enlarges 
to  several  times  its  original  size  and  becomes  decidedly  elongated.  The  first  division 
wall,  as  in  the  other  Marattiaceae,  is  transverse,  but  of  the  two  primary  cells  thus 
formed  the  hypobasal  one  divides  no  further,  or  only  once,  and  forms  a  short  sus- 
pensor which  pushes  up  into  the  neck  of  the  archegonium  whose  cells  become  more 
or  less  completely  disorganized  (fig.  114,  A).  The  next  division  wall  is  a  nearly 
median  one  in  the  epibasal  cell,  and  this  is  soon  followed  by  a  second  wall  in  each 


IMHKVi 


143 


.f  tlic 


basal  iills,  so  ihat  this  portiini  of  tin  cmhrvo  is  dunK-.l  into  foui  luarly 
equal  tiuadrants.  I  lure  is  sonic  cvickncc  that  these  are  tollowed  by  hoii/ontal 
octant  walls,  so  that  the  epibasal  region  is  thus  divided  into  octants  in  much  the  same 
fashion  as  obtains  in  the  whole  embryo  in  other  Marattiacea-  and  in  the  lepto- 
sporangiate  ferns.  How  far  these  divisions  are  constant  can  only  be  conjectured, 
owing  to  the  small  number  of  young  embryos  which  were  available.  The  elongated 
pear-shaped  embryo  in  Datura  appears  very  different  indeed,  in  these  early  stages, 
from  the  broadly  elliptical  and  much  depressed  embryos  of  corresponding  stages 
in  the  other  Marattiace;e  (fig.   i  14.  f ,  /_),  E). 


older  embryo.     X2cx3.    Section  B  is  a  nearly  median  ; 
A  is  the  next  section  in  the  series;  C  shows  the  suspensor,  sus. 

A  further  study  of  the  embryos  shows  that  all  of  the  lower  halt  of  the  epibasal 
region,  probably  that  derived  from  the  four  lower  octants — i.  e.,  the  four  octants 
that  were  in  contact  with  the  .suspensor — develops  into  the  foot,  while  all  of  the 
other  organs  of  the  embryo  (leaf,  stem,  and  root)  arise  from  the  four  terminal  octants. 

Quite  early  in  the  development  of  the  embryo,  there  appears  the  same  centrally 
placed  large  cell  which  we  have  observed  in  the  embryos  of  the  other  genera  and 
which,  as  we  have  seen,  probably  represents  the  primary  stem  initial.  Brebner 
concluded  that  a  single  initial  was  present  in  the  stem  of  Z).  simplicifolia  and  this  is 
true  of  the  three  species  e.xamined  by  me.    The  initial  of  the  stem  in  Daiura  becomes 


very  easily  seen  in  the  older  stages  and  is  perhaps  more  clearly  defined  than  it  is  in 
any  other  of  the  Marattiace;e.  Whether  or  not  this  cell  can  be  traced  back  to  one  of 
the  original  terminal  octant  cells  is  difficult  to  say,  but  it  is  quite  possible. 

No  single  initial  could  be  made  out  for  the  cotyledon,  and  it  seems  quite  likel}' 
that  the  position  of  the  cotyledon  is  not  always  exactly  the  same,  being  determined 
perhaps  by  the  position  of  the  embryo  with  reference  to  the  light  or  to  some  other 
factor.  The  cotyledon,  as  in  Marattia  and  Jngiopteiis,  first  appears  as  a  slight 
prominence  close  to  the  nearly  centrally  placed  stem  apex,  and  there  is  soon  visible 


144  THE    MARATTIALES 

a  group  of  actively  dividing  cells  which  constitute  its  growing  point,  but  no  one  of 
these  can  be  certainly  named  as  the  apical  cell  (fig.  117,  3).  The  embryo  now 
rapidly  increases  in  breadth  until  the  apex  is  almost  flat,  except  for  the  slight  pro- 
jection in  the  center,  where  are  situated  the  stem  apex  and  the  young  cotyledon. 
The  whole  embryo  at  this  stage  may  be  described  as  "top-shaped."  The  stem  and 
cotyledon  occupy  a  comparatively  small  portion  of  this  broad  terminal  area  and 
are  surrounded  by  a  ring  of  large  absorbent  cells,  physiologically,  at  least,  belonging 
to  the  foot  and  merging  insensibly  into  the  similar  cells  which  make  up  the  lower 
half  of  the  embryo. 


As  in  the  other  Marattiaces,  the  very  young  embryo  shows  no  trace  at  all  of 
the  root  and  this  appears  only  after  the  embryo  has  reached  a  comparatively  large 
size.  The  origin  of  the  root  is  exactly  the  same  as  in  the  other  genera  and  it  is  a 
strictly  endogenous  structure.  The  single  initial  cell  arises  deep  down  in  the  tissue 
of  the  embryo,  usually  below  the  cotyledon  and  probably  from  the  same  octant  as 
that  from  which  the  cotyledon  is  formed,  but  owing  to  the  displacement  of  the 
original  division  walls  this  can  not  be  determined  positively  and  it  may  be  that  the 
position  of  the  root  is  not  always  exactly  the  same.    The  apical  cell  of  the  root  soon 


i-iG.  119. — u.jamatcetisis. 
A.  Two  sections  of  an  advanced  embryo.      Xioo.     B.  Stem  apex  of  the  same  embryo.      X220. 

becomes  conspicuous,  but  it  does  not  usually  show  the  triangular  form  as  seen  in  a 
longitudinal  section,  but  appears  more  nearly  square,  as  in  Marattia.  This  root 
initial  cell  is  quite  variable  in  form,  but  more  commonly  it  appears  in  longitudinal 
section  with  a  truncate  base  (fig.  117,  r).  In  transverse  .section  it  approaches  the 
triangular  form,  but  is  more  or  less  irregular  in  outline.  The  lateral  segments  cut 
off  from  the  initial  cell  are  large  and  contribute  later  to  the  root  cap  as  well  as  to  the 
inner  root  tissues,  and  it  is  not  impossible  (as  Farmer  believes  to  be  the  case  also 


III.     IMHK^I 


145 


in  :lugi()[^trni)    that    sdiiutmu's   HKire  tliaii  out-  ot    tlicsf  tcimin.il  iills    tuiution    as 
tlic  apical  cell. 

As  soon  as  the  toot  apex  is  established  its  growth  is  veiy  ia|iiil  and,  as  in  the 
other  genera,  there  is  a  rapid  elongation  of  the  whole  embryo,  whose  vcitical  dianutci 
very  soon  becomes  greater  than  the  transverse  diameter,  and  ultimatel>  the  whole 
embrvo  becomes  veiy  much  elongated.  In  the  a.xial  region  of  the  embiyo  just  below 
the  stem  ape.x  there  is  a  marked  elongation  of  the  central  cells  which  might  at  first 
sight  be  taken  to  represent  the  central  vascular  cylinder,  but  these  elongated  cells  do 
not  give  rise  to  vascular  elements,  but  remain  as  elongated  parenchyma  and  belong 
really  to  the  pith.  Ihe  part  of  the  foot  which  lies  below  the  growing  root  apex 
acts  as  a  very  massive  root  cap  and  is  pushed  down  with  the  growth  of  the  toot  until 
the  latter  emerges  from  the  lower  side  of  the  piothalliiim.  The  cor\'Iedon  in  the 
meantime  grows  actively  ii|nvar(l   and   finally  penetrates  tlu'  piorhalliinn,  emerging 


on  the  upper  side.  The  growth  of  the  stem  is  slight  and  the  cotyledon  and  root  form 
nearly  a  straight  line,  as  in  the  other  Marattiaceae  and  in  Opluoglossum,  so  that  the 
young  sporophyte  may  be  described  as  bipolar.  The  equatorial  region  is  surrounded 
by  the  large  absorbent  cells  in  contact  with  the  prothallium  and  ail  of  these  may  be 
said  to  function  as  the  foot,  although  it  is  impossible  to  sa}'  how  much  of  this  tissue 
is  derived  from  the  original  foot. 


THE  ANATO\n  .AM)  HISTOLOGY  OF  THE  YOUNG  Sl'OROl'H^' IK. 

The  young  sporophyte,  at  the  time  the  root  emerges  from  the  prothalliinii,  is 
very  much  alike  in  all  of  the  genera  (figs.  io8,  iii,  I2i).  The  cotyledon  at  this 
stage  is  a  thick,  conical  protuberance,  strongly  curved  inward  over  the  stem  apex, 
owing  to  the  more  rapid  growth  upon  its  outer  side.  Close  to  its  base  lies  the 
very  limited  growing  region  of  the  stem,  adjacent  to  which  is  the  rudiment  of  the 
second  leaf,  which  at  this  time  projects  very  slightly  above  the  level  of  the  stein  apex. 
The  cells  of  the  latter,  and  also  those  of  the  young  leaves,  are  evidentl)-  actively 
growing  cells  with  conspicuous  nuclei  and  are  quite  different  in  appearance  from  the 
large,  transparent  cells  that  compose  the  enlarged  mid-region  of  the  young  sporo- 
phyte. This  is  largely  made  up  of  the  original  tissue  of  the  foot,  but  this  tissue  merges 
insensibly  into  the  basal  region  of  the  cotyledon  and  the  upper  part  of  the  root, 
these  two  organs  forming  in  their  growth  almost  a  straight  line.  \\'hether  or  not 
we  term  this  middle  region  of  the  young  plant  the  "stem,"  it  must  be  borne  in 
mind  that  it  does  not  arise  from  the  activity  of  the  extremely  limited  meristem, 
forming  the  true  stem  apex.  The  young  sporophyte  is  traversed  by  a  single  conspic- 
uous vascular  bundle  which  extends  through  the  cotyledon  and  root  without  intei- 

10 


146 


THE    MARATTIALES 


riiption,  and  it  is  quite  impossible  to  say  just  exactly  where  the  point  of  junction  is. 
In  Angiopteris  elongated  tannin  cells,  which  stain  very  strongly,  accompany  the 
vascular  bundle,  both  in  the  root  and  cotyledon;  but  these  are  either  entirely  wanting 
or  but  slightly  developed  in  Marattia  and  are  quite  absent  from  the  young  sporophyte 
at  this  stage  in  the  other  genera.  In  the  relation  of  the  primary  root  and  leaf,  there- 
fore, the  embryo  of  the  young  sporophyte  in  the  Marattiaceae  shows  a  most  striking 
resemblance  to  the  condition  found  in  Ophtoglossum  moluccaiium.  The  cotyledon, 
as  in  Ophioglossum,  is  not  to  be  looked  upon  as  an  appendage  of  the  stem,  but  as  an 
organ  siti  generis. 

Almost  as  soon  as  the  second  leaf  is  recognizable,  there  is  evident,  connecting 
it  with  the  primary  vascular  strand,  a  short  group  of  procambium  cells,  and  the 
stem  apex  is  seen  to  occupy  the  space  between  these  two  leaf  traces.  No  procambium 
IS  developed  in  the  stem  above  the  junction  of  the  leaf  traces,  hut  the  inner  cells,  derived 
from  the  apical  meristem,  contribute  solclv  to  the  medullary  tissue  of  the  sporophyte 

(hg.izuJ).  _  '  ' 

..h 


Fig.  ill.—Dim.cajamaicens 

15. 

Large  embryo,    cot 
Median  section  of  ( 

,  cotylcdo: 
;otyIedon; 

n;  I',  second  leaf.    X50. 
h,  epidermal  scale.     X95. 

C.  Second  leaf. 

D.  Trichomes  f 

X,5o.          ^ 
rom  apical  region. 

The  first  tracheary  tissue  arises  in  the  mid-region  of  the  young  sporophyte  and 
consists  of  a  group  of  short  reticulate  tracheids.  From  this  point  the  development 
of  the  tracheary  tissue  proceeds  upward  into  the  cotyledon  and  downward  into  the 
root.  The  single  strand  of  tracheary  tissue  in  the  cotyledon  is  seen  to  be  continuous 
with  one  of  the  xylem  masses  of  the  diarch  root.  The  second  xylem  of  the  root  arises 
somewhat  later  and  is  connected  with  the  xylem  of  the  second  leaf.  This  second 
xylem  mass  is  decidedly  smaller  than  the  first  one,  at  least  in  Dancea,  where  I  have 
studied  this  point  carefully,  and  an  examination  of  the  other  genera  points  to  a 
similar  inequality  in  the  xylems  of  these  as  well,  but  this  may  not  always  be  the  case. 

THE  COTYLEDON. 

The  cotyledon  at  a  very  early  period  bends  strongly  over  the  stem  apex,  very 
much  as  it  does  in  Botrychium  virginianum,  and  very  soon  afterwards  begins  to 
flatten  out,  so  as  to  indicate  the  separation  of  the  lamina  from  the  petiole.  The 
flattening  of  the  apex  is  followed,  in  many  cases  at  least,  by  a  true  dichotomy,  which 
is  soon  repeated,  so  that  the  lamina  becomes  fan-shaped,  with  a  strictly  dichotomous 
venation  (fig.  87,  G,  H;  fig.  127).  This  shows  especially  well  in  Marattia  douglasii. 
In  M.  sambucina  (fig.  87,  C)  the  cotyledon  is  more  nearly  orbicular  than  in  M. 
douglasii,  but  the  venation  indicates  a  similar  early  dichotomy  of  the  apex. 

In  Angiopteris,  the  form  of  the  cotyledon  is  extremely  variable  (fig.  124). 
Farmer  states  that  it  has  a  distinct  midrib  extending  to  the  apex  of  the  cotyledon 


THF    YOUNG    .SPOROPHYTF  147 

ami  that  the  seionclaix'  \tiiis  aii'  |iinnattly  aiiangtcl  with  leti-ieiuc:  to  the  midrib. 
These  later  veins,  however,  may  show  clichotonious  branching.  I  made  an  e.xamina- 
tion  of  a  considerable  number  of  young  sporophytcs  collected  at  the  same  place  where 
Professor  Farmer  secured  his  specimens,  but  very  few  of  the  plants  that  I  collected 
siioweci   this  pinnate  \enation  in   the  cotvUdon.  although   it  is  usualh'  conspicuous 


11^  sporophyte  of  .1 
to  tlie  gametopl 


Young   sporophyte  of   Kaulju 

gametophyte,/ir.   X2. 
Cotyledon  from  another  plant . 
A  later  leaf;   ir,  stipule.      /  i . 


in  the  second  leaf.  Figure  124,  6",  shows  drawings  of  a  number  of  the  forms  from 
my  collection,  showing  the  variation  from  a  strictly  pinnate  to  a  perfectly  dichoto- 
mous  venation.  Many  of  them  show  an  intermediate  venation,  but  with  very  few 
exceptions,  even  where  a  midrib  was  present,  this  was  forked  at  the  apex,  indicating 


F.r..  ,24. 

A.  Young  sporophyte  of  .In^lopicrisj  with  three  leaves. 

B.  Young  cotyledon.     X20. 

C.  Three  cotvh-dons,  showine  the  variation  in  form.     ; 


I  his  primar\ 
ung  leaf  (fig'. 


B)  wl 


.t    the 
re  thei 


ipe.K 
.■  wa,^ 


thai  llun   iiad  been  an  eai  I\- ilichotonn  .      Ibis  primar\   tli 
well  shown  in  a  section  thiough  a  vei 
(juestion  that  such  a  dichotomy  was  taking  phi 

In  Daiiira  there  is  much  the  same  variation  in  the  form  of  the  cot\leilon  as  in 
A)igioptcris.  Brebner's  figures  of  D.  stmplicifoUa  show  that  the  cotyledon  in  this 
species  has  a  midrib  with  two  lateral  veins  near  the  base,  but  sometimes  the  midrib 
forks  at  the  summit,  indicating  again  the  early  dichotomy  of  the  cotyledon.     In  one 


148 


THK    MARATTIALES 


of  his  figures,  where  there  is  no  forking  of  the  mid-vein,  the  hiteral  veins  seem  to 
follow  the  margin  of  the  leaf  and  rejoin  the  central  vein,  thus  inclosing  two  large 
areoles  like  those  found  in  the  cotyledon  of  Kaiilfussi a;  no  mention  of  this,  however, 
is  made  in  the  text.    D.  jaNiaimisis  (fig.  125,  J)  shows  a  very  similar  form  and  vena- 


Four  young  bporophytes  still  M 
Young  cotyledon  of  D.  elliptka. 
An  older  cotyledon  of  D.  elliptii. 


tion,  but  the  cotyledon  is  larger  and  there  is  sometimes  a  forking  of  the  lateral  veins. 
In  this  species  also  there  may  sometimes  be  found  a  fan-shaped  lamina  with  true 
dichotomous  venation  like  that  of  Marattia,  but  as  I  had  httle  material  of  this 
species  I  can  not  say  how  common  this  form  is.    It  is  probable  that  an  examination 


lung  sporophyte  of  D.  jamtiicen 
lightly  enlarged,  i,  the  cotyledon 
ise  of  the  fourth  leaf,  showing  st 
cale,  K.      X20. 


ith    four   leavi 
.   </.  and   pelta 


of  a  large  series  of  young  plants  would  show  examples  of  the  same  type  ot  cotyledon 
as  in  the  other  species.  The  cotyledon  of  Z).  elliptica  (fig.  125,  B,  C)  is  of  much  the 
same  form  as  that  of  D.  jamaicensis,  but  the  cotyledon  is  larger  as  a  rule  and  the 
venation  may  be  more  complex,  although  conforming  to  the  same  general  type. 


II F    YOL'NC    srOKOI'HYTI-: 


149 


The  cotyledon  in  Ka/il/nsMti  (lig.  \z^)  is  s|iatiilatL-  in  loim  and  not  unlike-  that 
of  DciiKva  in  shape  and  also  closely  resembles  in  outline  the  broader  leaf  forms  of 
Ophioglossiirn  tuoliicctinurri.  I  he  resemblance  to  the  latter  is  much  increased  by 
the  venation,  which  is  reticulate  and  extraordinarily  like  that  of  the  cotyledon  of 
Ophioglossum.  As  in  Ophioglossuni,  there  is  usually  a  mid-vein,  but  this  is  not, 
however,  noticeably  thicker  than  the  laterals.  The  latter,  instead  of  extending 
free  to  the  edge  of  the  leaf,  are  connected  at  their  distal  ends  with  the  mid-vein  so 
as  to  inclose  more  or  less  elongated  arcoles.  The  central  vein  does  not  extend  to  the 
tip  but,  as  in  Dancea,  divides  into  equal  branches  which  join  above  so  as  to  inclose 


ityledon  of  Marattia  dou^lasli.     X260. 
of  cotyledon.     X300. 


onchti\  veins  shows  that  theii 
'ins  of  the  other  Marattiace;e 
rgin  of  the  leaf,  or  more  rareh 


a  terminal  areole.  A  careful  examination  of  the  s 
divisions  are  really  dichotomous,  as  in  the  lateral 
and  some  of  the  ultimate  branches  ma\'  reach  the  n 
they  may  end  freely  within  the  areoles. 

As  the  cotyledon  develops  there  is  more  or  less  elongation  of  the  petiole,  which, 
however,  very  seldom  exceeds  the  lamina  in  length.  The  petiole  is  usually  more  or 
less  deeply  channeled  upon  its  inner  face.  In  Marattia  doiiglasii  (fig.  133)  the  base 
of  the  cot\  ledon  is  much  enlarged   just  above  the  le\el  of  the  stem  apex,  which  is 


A.  Section  of  la 

B.  A  young 

C.  An  older  one. 

thus  almost  inclosed  in  a  sort  of  cleft  in  the  base  of  the  cotyledon,  very  much  as  it  is 
in  the  case  oi  Botrychiitm  or  H elmijitliostachys.  In  Anginpteris  there  is  but  slight 
contraction  at  the  base  and  the  stem  apex  forms  a  strongly  oblique  surface,  hardl}' 
covered  at  all  by  the  base  of  the  cotyledon.  The  base  of  the  cotyledon  is  still  more 
conspicuously  hollowed  out  in  Dantrn  and  especially  in  Kaiilfiissia  (figs.  136.  137), 
and  in  the  latter  there  is  a  circular  ridge  completely  surrounding  the  stem  apex, 
exactly  as  is  the  case  in  the  young  bud  in  Ophioglossuni  tnoliircarnnn.  Traces  ot 
this  ridge  can  be  seen  also  in  Damra  and  Marattia,  but  this  is  much  less  conspicuous 
than  in  Kaiilfiissia.  In  the  latter  this  cavity  is  especially  marked,  .so  that  one  might 
almost  speak  of  a  stipular  sheath,  and  this  resemblance  to  Opiiioglossiint  in  the 


150 


THE    MARATTIALES 


relation  of  the  leaf  base  and  stem  apex,  especially  in  connection  with  the  Ophio- 
glossiim-WkQ  venation  in  Kaulfussia,  is  not  without  significance  in  its  bearing  upon 
a  possible  relationship  between  the  Marattiaceae  and  the  Ophioglossaceae. 

In  all  of  the  genera  the  lower  part  of  the  cotyledon  and  sometimes  the  stem 
apex  are  more  or  less  covered  with  hairs  and  scales.  I  hese  are  less  abundant  in 
Marattia  and  Angiopteris,  where  they  are,  for  the  most  part,  short  hairs  whose 
terminal  cells  contain  a  great  deal  of  tannin  and  stain  very  strongly.  In  Kaulfussia, 
and  especially  in  Dancea,  conspicuous  scales  of  peculiar  form  are  abundant. 


^"^^"^^^^ 


A.  Section  near  base  of  lamina  of  cotyledon.     X75.         D.  An  older  stoma.      X200. 

B.  Part  of  the  lamina,  jf,  stoma.     X200.  E.  Cross-section  of  a  peltate  scale,  from  young  cotyledon.    X200. 

C.  Young  stoma. 

In  Marattia  dougJasii  the  nearly  cylindrical  petiole  is  somewhat  channeled  on  its 
inner  side  and  the  single  and  nearly  centrally  placed  vascular  bundle  appears  almost 
circular  in  section.  The  xylem  forms  a  somewhat  crescent-shaped  body,  completely 
inclosed  by  the  phloem,  but  the  phloem  is  less  developed  upon  the  inner  side  and 
the  bundle  closely  approaches  the  collateral  type.  Tannin  cells  occur,  but  are  not 
so  conspicuous  as  they  are  in  Angiopteris.  The  lamina  of  the  cotyledon  is  similar 
in  structure  to  that  of  the  latter,  the  leaves  differing  mainly  in  the  much  smaller 
development  of  the  mesophyll,  which  is  often  reduced  to  a  single  layer  of  cells  (fig. 

127,5).  The  smaller  veins  have 
the  xylem  reduced  to  a  few — 
one  to  three — small  tracheids 
situated  upon  the  upper  side  of 
the  bundles,  so  that  the  bundles 
are  strictly  collateral.  Stomata 
of  the  ordinary  form  occur  upon 
the  lower  surface  of  the  leaf  and 
these  sometimes  show  a  series 
of  concentrically  arranged  cells 
about  them. 

The  petiole  of  the  cotyledon 
in  Angiopteris  resembles  in  sec- 
tion that  of  Marattia,  but  it  is  slightly  winged  (fig.  130),  and  the  tannin  cells  adja- 
cent to  the  vascular  bundle  are  more  conspicuous  than  in  Marattia. 

In  Kaulfussia  (Rg.  137,  C),  where  the  petiole  is  stouter  than  in  the  other  genera, 
the  section  is  more  nearly  circular  than  in  Angiopteris,  but  it  is  also  slightly  winged, 
these  wings  being  developed  almost  to  the  proportions  of  stipules  at  the  contracted 


HK    VOUNG 


151 


basal  portion,  llie  vascular  bundle  lias  a  greater  development  of  xyleni  than  in  the 
other  genera  and  the  xyleni  forms  a  band  of  considerable  extent  in  the  oval  section  of 
the  bundle.  The  structure  of  the  bundle  is  concentric,  but,  as  in  other  cases,  the 
phloem  is  better  developed  upon  the  outer  side.  Below  the  free  base  of  the  cotyledon, 
where  the  trace  enters  the  stem,  there  is  a  reduction  of  the  inner  phloem,  or  the 
inner  phloem  entirely  disappears,  and  the  bundle  there  becomes  truly  collateral.  No 
definite  endodermis  can  be  recognized  and  the  tannin  cells  found  in  the  cor\le(lon 
of  Angiopteris  are  quite  absent. 


A.  Section  of  petiole  oi 

B.  The  vascular  bundle.     X200. 

C.  Section  of  a  peltate  scale.     X75. 

The  section  of  the  petiole  of  the  cotyledon  in  Danaa  (fig.  131)  is  nearly  cir- 
cular, and  the  wings  found  in  the  other  forms  are  almost  entirely  obliterated.  The 
ground  tissue  is  composed  of  undifferentiated  parenchyma,  with  no  trace  of  tan- 
nin cells.  The  vascular  bundle  is  circular  in  outline,  with  a  small  group  of  three 
or  four  tracheids  placed  somewhat  toward  the  inner  side  of  the  bundle,  but  sepa- 
rated from  the  outside  by  about  two  rows  of  cells,  probably  phloem,  but  not 
showing  any  differentiation.  Small  protophloem  elements,  staining  darkly,  can 
be  seen   upon  the  dorsal  side  of  the  bundle  and  an  occasional  similar  cell  can   be 


A.  Two  longitudinal  sections  of  a  somewhat  older  sporophyte  of  A/,  doiigjaiii. 

B.  Apical  region  of  stem,  showing  apical  cell  and  second  leaf.  /".     X2oa 

seen  toward  the  ventral  side,  but  most  of  the  ventral  surface  is  destitute  of  these. 
1  he  petiole  broadens  at  its  base,  becoming  flattened,  and  in  this  region  the  inner 
phloem  disappears  and  the  bundle  becomes  collateral,  as  it  is  in  Ophioglossum.  The 
tracheary  tissue  of  the  cotyledon  in  all  of  the  Marattiacerr  is  composed  of  slender, 
reticulately  marked  tracheids,  like  those  of  Ophioglosstim.     Sieve  tubes  are  prob- 


152  THE    MARATTIALES 

ably  present  in  the  phloem,  but  in  material  mounted  in  Canada  balsam  the  sieve 
tubes  are  very  poorly  differentiated. 

Upon  the  cotyledon  as  well  as  upon  the  later  leaves  in  Dnna-a  very  character- 
istic peltate  scales  are  developed.  These  arise  as  single  club-shaped  cells,  the 
swollen  end  of"  which  is  cut  off  by  a  cross  wall.  In  the  upper  cell,  which  broadens 
rapidly,  a  series  of  vertical  walls  arises,  sometimes  arranged  very  regularly  (fig. 
129,  E).  In  the  case  figured  there  had  evidently  been  two  median,  intersecting  walls, 
so  that  the  cells  were  arranged  in  a  somewhat  quadrant  fashion;  more  commonly 
the  divisions  are  less  regular  and  the  cells  increase  considerably  in  size  by 
further  divisions.  A  section  of  an  older  scale  may  be  seen  in  fig.  131,  C.  Stomata 
are  developed  upon  the  lower  surface  of  the  cotyledon  in  all  of  the  Marattiaceae. 
These  have  already  been  referred  to  in  the  case  of  Marattia,  and  in  Angiopteris 
they  are  very  similar  to  those  found  in  Marattia.  In  Dancea,  previous  to  the 
formation  of  the  stoma,  there  are  several  preliminary  divisions,  the  cells  being  cut 


off  in  a  spiral  fashion,  the  last  division  resulting  in  the  formation  of  the  mother  eel 
of  the  stoma  (fig.  129,  C).  The  complete  stoma  appears,  therefore,  surrounded  by 
a  series  of  somewhat  concentrically  arranged  accessory  cells  (fig.  129,  D).  Similar 
accessory  cells,  but  much  less  developed,  can  be  recognized  in  Marattta  also. 

The  stomata  of  Kaiilfussia  have  long  been  known  for  their  great  size  and  the 
fact  that  they  form  permanently  open  pores,  a  peculiarity  already  developed  in  the 
stomata  of  the  cotyledon.  These  are  very  much  larger  than  those  of  the  other  genera 
and  can  be  readily  recognized  by  the  naked  eye  as  little  dots.  The  guard  cells 
become  very  large  (fig.  128)  and  strongly  curved,  so  that  the  stoma  appears  almost 
circular  in  outline,  with  a  very  large  permanently  open  central  pore.  This  large 
pore  is  surrounded  by  concentrically  arranged  series  of  cells,  suggesting  that  the 
mother  cell  of  the  stoma  is  cut  off  very  much  as  in  Dana-a,  but  material  was  want- 
ing for  a  thorough  investigation  of  this  point. 


THE    YOUNG    Sl'OROPHVTI 


153 


THE  STKM  or  THE  VOINt;  SPOKDPHVTE. 

The  stem  apex  projects  very  little  or  nor  at  all,  and  occupies  but  a  limited  area 
close  to  the  base  of  the  cotyledon.  Its  outer  surface  is  nearly  horizontal,  except  in 
Angtoptcris,  where  it  is  generally  strongly  inclined  (fig.  134).  I  here  probably  is 
always  a  single  apical  cell.  Segments  are  cut  off  from  the  sides,  and  very  often  also 
inner  segments,  where  the  base  of  the  apical  ceil  is  truncate.  'Ihe  lateral  segments 
also  have,  cut  off  from  their  inner  faces,  cells  which  contribute  to  the  growth  in  length 
of  the  stem,  which  remains,  however,  very  short  in  the  young  sporophyte,  the  leaves 
being  very  much  crowded  together.  As  we  have  already  stated,  no  central  cylinder 
properly  belonging  to  the  stem  can  be  demonstrated  at  this  time,  all  of  the  procambial 


,  Stem  apex,  showing  single  apical  cell. 
.  Second  leaf,  /''.of  same  sporophyle. 


Nearlv  median  sect 
/-,  second  le.if;  m,  r 
Inphyte.     X  about ; 


of  a  young  sporophyte  of  Ktiulfuss 
ilage  ducts;  at,  stem  apex;  fit 


tissue  belonging  either  to  the  cotyledon  or  to  the  root.  In  the  older  embryo  of 
Marattia  douglasii  the  apex  of  the  stem  (fig.  139.  B)  is  occupied  by  a  group  of  rela- 
tively large  cells,  which  at  first  sight  seem  to  be  pretty  much  alike;  but  a  careful 
examination  of  these  makes  it  probable  that  one  of  them  may  be  considered  as  the 
real  initial  cell.  This,  in  cross-section,  appears  almost  square  and  shows  a  fairly 
regular  segmentation.  While  it  must  be  said  that  the  segmentation  is  not  so  regular 
that  one  can  assert  without  (juestion  that  all  of  the  meristem  is  really  due  to  the 
activity  of  a  single  cell,  I  believe  that  this  is  probably  the  case. 

My  own  investigations  of  the  stem  apex  in  Angtopteris  have  led  to  the  conclusion 
that  there  is  a  single  initial  cell  here  also  in  the  young  sporophyte,  although  Farmer 


154 


THE    MARATTIALES 


in  his  earlier  studies  of  this  plant  failed  to  find  a  single  initial  cell;  however,  in  a 
more  recent  paper  (Farmer  3)  he  has  decided  that  a  single  apical  cell  is  present  in 
the  young  sporophyte  of  Angiopteris,  and  he  gives  figures  of  this.  In  longitudinal 
section  (fig.  134)  the  apical  cell  appears  oblong,  with  a  markedly  truncate  base, 
while  in  transverse  section  it  is  imperfectly  triangular  in  outline.  The  apical  cell 
of  the  stem  in  Kaiilfussia  (fig.  136,  C)  is  usually  somewhat  broader  than  it  is  in 
Angiopteris,  and  closely  resembles  that  of  Ophioglossum  nioluccanum.  It  has  a 
broadly  truncate  base  and  is  somewhat  narrowed  above.  In  transverse  section  it 
approaches  the  triangular  outline  of  the  apical  cell  in  Ophioglossum,  but  the  seg- 
mentation is  less  regular  and  in  this  respect  it  is  not  unlike  that  oi  Angiopteris.  The 
stem  apex  was  examined  in  three  species  of  Datia-a,  all  of  which  seemed  to  agree 


A,  B.  Two  transverse  sections  of  a  young  sporophyte,  above 
level  of  stem  apex,  showing  closed  sheath  formed  by 
base  of  cotyledon.    /^,  second  leaf.     X50. 


Transverse  section  of  petiole  of  cotyledon.     X 
Vascular  bundle  of  cotyledon,  more  enlarged. 


closely  in  the  form  of  the  apical  cell,  which  is  much  more  definite  in  Danaa  than  it 
is  in  any  of  the  other  genera.  Brebner's  account  and  figure  of  the  apical  cell  in 
D.  simplicifolia  agree  closely  with  my  own  preparations  of  Z).  eUiptica,  D.  jerimani, 
and  D.  jamaicensis. 

The  apical  cell  (fig.  140,  A),  seen  in  longitudinal  section,  is  very  deep  and, 
unlike  that  of  the  other  genera,  is  not  usually,  at  least,  truncate  below,  but  pointed, 
so  that  it  closely  resembles  in  form  that  of  Botrychinm  or  HeJmintbostachys.  In 
transverse  section  it  also  usually  appears  triangular,  so  that  it  is  tetrahedral  like 
that  of  Botrychinm.  While  the  segmentation  is  somewhat  less  regular  than  in 
Botrychinm,  nevertheless  the  limits  of  the  younger  segments  can  be  followed  without 
much  difficulty,  especially  in  longitudinal  sections,  although  the  exact  sequence  of 
the  divisions  in  the  segments  themselves  did  not  seem  to  be  absolutely  regular. 

In  all  of  the  species  the  tissue  derived  from  the  inner  cells  of  the  segments  of 
the  apical  cell,  or  cut  off  from  the  base  of  the  apical  cell  itself,  remains  as  undif- 
ferentiated parenchyma  and  contributes  only  to  the  central  pith  of  the  stem.     I^'xcept 


THE    YOUNG   SPOROPHYTF. 


155 


that  the  leaves  arise  from  the  segments  of  the  apical  cell  of  the  stem,  and  their 
tissues  are  therefore  indirectly  derived  from  the  stem  apex,  we  may  say  that  the  stem 
apex  takes  no  part  in  the  differentiation  of  the  fibro-vascular  system,  which  in  the 
young  sporophyte  is  composed  entirely  of  the  leaf  and  root  traces. 


Only  a  small  number  of  sections  of  the  primary  root  were  obtained  in  Marattia 
donglasii,  and  these  showed  some  variation,  so  that  it  is  not  possible  to  state  posi- 
tively what  is  the  typical  form  of  its  apical  cell,  but  there  is  no  question  that  the 
primary  root  grows  from  a  single  initial  cell,  as  in  the  other  genera.  In  longitudinal 
section  it  appears  oblong,  with  a  broadly  truncate  base  from  which  segments  arise, 
as  well  as  from  the  lateral  faces.       There  seem  to  be  regularly  four  sets  of  lateral 


.\.  Nearly  median  section  of  a  young  sporophyte  of  DatnEa  jatt 

B.  Another  section  of  same,  passing  through  second  leaf,  /" 

C.  Section  of  another  similar  sporophyte  cut  at  right  angles  to  that  shown 

of  bundles  of  cotyledon  and  primary  root.     /)r,  gametophyte;  tc,  scales. 

segments,  although  cross-sections  of  the  apical  cell  sometimes  appear  almost  trian- 
gular. The  root  cap  is  formed  in  partffrom  segments  derived  from  the  outer  face 
of  the  apical  cell,  in  part  from  similarjsegments  cut  off  from  the  outer  portion  of 
the  youngest  lateral  segments  of  the  apical  cell.  The  central  cylinder  of  the  root 
is  formed  in  part  from  the  basal  segments  of  the  apical  cell,  but  the  lateral  seg- 
ments also  contribute  to  it  (fig.  141,  D). 

In  Angiopteris  (fig.  ill,  C)  the  apical  cill  in  rhe  earlier  stages  of  the  root  may 
appear  triangular  in  longitudinal  section,  bur  in  rht-  later  stages  it  is  usualh'  moie  or 
less  truncate. 

The  primary  root  in  Kuulfussni,  in  the  few  cases  where  satisfactory  sections 
were  made  of  it,  did  not  show  the  tetrahedral  apical  cell,  but  this  was  truncate  at  the 
base  and  in  cross-section  appeared  four-sided  (fig.  142).  In  this  respect  it  seems  to 
approach  M/irnttia.     The  primary  root  in  all  of  the  Maratriace:f  is  ordinarily  diarch; 


156  THE    MARATTIALES 

the  Statement  (Campbell  3,  page  14)  that  in  Morattia  douglasii  the  primary  root 
is  tetrarch  I  have  found  to  be  based  upon  a  mistake,  the  root  which  was  so  de- 
scribed not  being  the  primary  root,  but  evidently  one  of  the  later  ones.     I  have 

occasionally  found  very  strong  plant- 
lets  in  Dancea,  where  the  primary 
root  was  triarch,  as  it  sometimes  is 
in  Botrychium,  and  very  commonly  is 
in  Helminthostachys;  but  such  spe- 
cimens are  not  common.  I  he  root 
bundle  is  bounded  by  a  conspicuous 
endodermis,  whose  cells  show  very 
plainly  the  characteristic  radially 
thickened  bands  (figs.  143,  en;  144). 
The  endodermis  gradually  loses  its 
definite  appearance  at  the  junction 
of  the  root  and  leaf  bundles,  and  I 
have  not  been  able  to  recognize  it 
above  the  level  of  the  base  of  the 
dousia^ii.  cotyledon,  although  it  is  not  at  all 
impossible  that  with  proper  staining 
it  might  be  traced  further  up. 

THE  SECOND  LEAF. 

The  second  leaf  begins  to  develop  while  the  cotyledon  is  still  small,  and  by  the 
time  the  latter  ruptures  the  overlying  prothallium  tissue  the  second  leaf  is  clearU' 
evident  as  a  flattened  cone,  closely  resembling  the  early  stage 
of  the  cotyledon.  In  KaulfussKi  the  second  leaf  arises  quite 
close  to  the  cotyledon  and  on  the  same  side  of  the  stem  apex, 
so  that  the  dorsiventral  character  of  the  stem  is  already  indi- 
cated at  this  early  stage  of  development.  In  the  other  genera 
the  second  leaf  arises  nearly  opposite  the  cotyledon,  but  not 


Fig.  139. 
Transverse  section  of  a  young  sporophv 

sr,  stem  apex.     X150. 
The  stem  apes.     X360. 


exactly  so,  and  the  subsequent  leaves  form  a  spiral,  and  for  a  time  at  least,  except 
in  Kaiilfiissia,  the  anatomy  of  the  shoot  is  radial.  This  radial  arrangement  is 
retained    permanently  in  Mnrattia   and   Atigiopteris   and    also  in  some  species  of 


Till-;  voi'N(;   spoKoi'inri: 


157 


Ddihiti,  i:.  ^.,  I),  rlli/'t/tii;  Inir  in  D.  ifinnuin  ;mcl  in  /).  jininii ,i)isi s,  ws  wvW  ;is  in 
most  of  the  other  species,  the  stem  hii;ill\-  heeonus  dorsiventral.  ;is  it  is  from  the 
first  in  Kaiilfiissia. 

'\he  development  of  tlie  seeond  leaf  is  marked  h)  an  increased  activit)  in  the 
apical  meristem,  (jiiite  close  to  the  apical  cell,  and  it  is  clear  that  the  leaf  arises  from 
the  younijer  sejjments,  hut  it  is  impossihie  to  state  exactly  what  the  relation  of  the 
xoimij  leaf  is  to  the  yoimj^er  seijments  of  thi  apical  cell,  or  to  say  whether  the  whole 


A-C.  Three  transverse  sections  o(  primary  root  of  Marattia  douglwii. 
D    Longitudinal  section  of  apex  of  primary  root. 

of  the  loaf  is  the  derivative  of  a  single  segment.  When  the  young  leaf  can  first  be 
distinguished  it  is  elevated  very  slightly  above  the  level  of  the  stem  apex  and  its 
growing  point  is  composed  of  a  group  of  columnar  cells.  Sometimes,  especially  in 
DaiKra,  there  may  be  recognized  near  the  center  of  this  group  of  cells  a  single, 
somewhat  larger  one,  which  may  be  interpreted  as  a  single  apical  cell,  but  this  is  not 
always  recognizable. 


A,  longitudinal,  B, 
C.  Apex  of  second 
D    Transverse  sect 

Kven  before  there  is  any  noticeable  projection  of  the  leaf  rudiment,  there  is 
developed  beneath  it  the  beginning  of  the  short  strand  of  piocambium  which  is  to 
form  its  vascular  bundle,  and  this  can  be  followed  downward  to  a  point  below  the 
stem  apex,  where  it  joins  the  trace  from  the  cotyledon.  Above  this  junction  there  is 
no  evidence  of  procambium  tissue  extending  into  the  stem  apex,  but  the  whole 
tissue  lying  between  the  junction  of  these  two  primary  vascular  bundles  and  flu- 
apical  meristem  of  the  stem  is  made  up  of  undifferentiated  parench\ma. 

The  outer  surface  of  the  stem  apex  may  be  nearly  horizontal  or  (especially  in 
Angi(jpteris)  it  may  be  strongly  inclined  and  a  single  fairly  conspicuous  initial  cell 


158 


THE    MARATTIALES 


may  usually  bt  recognized  without  difficulty.  Iliis  ceil  is  usually  quite  deep  and 
in  all  of  the  genera  except  Dantea  has  a  truncate  base  in  longitudinal  section.  In 
Daticea,  however,  the  base  is  usually  pointed  and  the  cell  closely  resembles  the  corre- 
sponding cell  in  Botrychtum,  or  the  typical  leptosporangiate  ferns.  The  growth  of 
the  stem  is  usually  rather  slow  and  the  leaves  of  the  young  plant  are  much  crowded. 

In  all  of  the  forms  e.xamined,  the  tissue  derived  from  the  inner  cells  of  the 
segments  and  from  the  basal  segments  of  the  apical  cell,  where  such  segments  were 
formed,  remained  as  undifferentiated  parenchyma  and  contributed  only  to  the 
internal  pith  of  the  stem.  Except  that  the  leaves  arise  from  the  segments  of  the 
apical  cell  of  the  stem  and  all  of  their  tissues  are  therefore  indirectly  derived  from  it, 
the  stem  apex  of  the  young  sporophyte  takes  no  part  at  all  in  the  development  of 
the  fibrovascular  system  of  the  stem,  which,  except  for  the  bundles  of  the  roots,  is 
entirely  composed  of  the  leaf  traces. 

The  second  leaf  in  Angiopterts  usually  shows  a  pretty  well-defined  but  slender 
midvein,  which  may,  however,  fork  at  the  apex,  and  this  is  true  also  of  the  third  leaf. 
It  is  in  the  third  leaf,  both  in  Marattia  and  Angiopteris,  that  the  characteristic 
stipules  are  first  developed.    These  appear  as  lateral  wing-shaped  bodies  close  to  the 


A.  SectioD  of  primary  root  of  Dai 

B.  The  vascular  bundle.     X175. 

C.  Triarch  bundle  from  a  primary 


jainatcensis. 
cndodermis. 
)t  of  D.  elliflii 


base  of  the  petiole,  partially  inclosing  the  next  youngest  leaf  and  the  stem  apex. 
The  third  leaf  in  Angiopteris  and  several  others  succeeding  it  assume  a  more  and 
more  pronounced  lanceolate  form  with  a  prominent  midrib  and  pinnately  arranged 
lateral  veins  which  usually  fork  once.  The  margin  of  the  leaf  is  serrate.  After 
several  of  these  lanceolate  leaves  have  been  developed,  leaves  are  formed  in  which 
the  base  is  provided  with  auricles,  and  these  gradually  pass  into  the  next  type  of  leaf, 
which  is  ternate,  the  terminal  leaflet  being  very  much  larger  than  the  lateral  ones 
(plate  13,  figs.  4,  5).  These  ternate  leaves  then  pass  by  intermediate  stages  into 
the  pinnate  form  of  the  leaves  of  the  adult  plant. 

In  Kaulfussia  the  second  and  third  leaves  closely  resemble  the  primary  one, 
except  that  they  are  somewhat  larger  (fig.  123).  The  second  leaf  develops  well- 
marked  stipules  which  are  found  in  all  of  the  later  leaves.  The  earlier  leaves  do  not 
show  a  definite  midrib,  though  there  is  usually  a  delicate  midvein  at  the  base  of  the 
lamina,  but  this  vein  forks  usually  about  half-way  up.  In  the  older  leaves  (fig.  123, 
C)  there  is  developed  a  stout  midrib,  from  which  extend  distinct  pinnately  arranged 
lateral  veins,  much  as  in  Angiopteris,  but  these  lateral  veins  are  connected  by  a 
system  of  anastomosing  veins,  so  that  the  leaf  most  strikingly  resembles  that  of  a 
typical  Dicotyledon.  It  is  not  until  a  very  late  period  that  the  leaves  in  Kaulfussia 
assume  the  compound  form  of  the  older  plant  (plate  11,  fig.  i). 


THF    YOUNG    SPOROPHVTF 


159 


In  Diuhi-a  a  dozen  or  more  kavcs  may  be  tormeil  before  there  is  any  brancliinij 
of  tile  lamina.  While  the  cotyledon  may  show  an  approach  to  the  pinnate  venation 
of  the  older  leaves,  there  is  almost  always  a  dichotomy  of  the  apex  of  the  slender 
midvein,  and  this  is  generally  true  also  for  a  number  of  the  subse(]uent  leaves, 
although  in  these  later  leaves  the  midrib  becomes  well  marked  and  the  lateral  veins 
are  developed  apparently  monopodially.  In  D.  siniplicifolid  the  leaves  remain 
permanently  unbranched,  but  in  all  of  the  other  species  the  later  leaves  are  once 
pinnate.  The  intermediate  leaves  have  the  ternate  form  found  in  Marattia  and 
Aiigiopteris,  and  after  a  few  of  these,  about  two  or  three,  have  been  formed,  five 
foliate  leaves  appear  and  the  number  of  leaflets  gradually  increases,  as  new  leaves 
are  formed,  until  the  full  number  of  leaflets  is  developed.  The  early  ternate  leaves 
often   have  the  terminal  leaflet  much   larger  than   the  lateral  ones,   and   the    leaf 


closely  resembles  the  corresponding  stages  in  Augiopteris.  The  petiole  in  most 
species  is  more  or  less  obviously  winged.  In  Daua-a  the  stipules  are  (sometimes,  at 
least)  not  formed  until  the  fourth  leaf.  In  the  fourth  leaf  (fig.  126,  B),  however, 
they  are  well  developed,  appearing  as  two  conspicuous  wing-like  organs  with 
serrate  edges. 

In  all  of  the  genera  there  is  a  root  formed  for  each  leaf  in  tlu'  carh\i  stages  of 
the  sporophyte,  but  how  late  this  continues  was  not  determined.  In  the  older 
sporophyte  more  than  one  root  may  be  formed  for  each  leaf.  In  Kaulfitssia  the 
second  root  is  developed  earlier  than  in  the  other  genera,  beginning  to  develop  while 
the  second  leaf  is  still  very  small,  and  in  general  the  roots  in  K  aid  fuss  in  seem  to 
develop  earlier  than  in  the  other  genera.  The  second  root  is  especially  late  in 
developing  in  Dmura,  the  very  first  rudiment  of  the  root  making  its  appearance 
between  the  first  and  second  leaves,  after  the  latter  is  aliead\  (uiire  will   advanced. 


160  THU    MARATTIALKS 


111.    IHK  OLDER  SPOROPHVIK. 


Ihe  vasculai  s)  stem  ot  the  adult  sporophyte  in  the  Marattiace;e  is  extremely 
complex,  especially  in  the  larger  species  of  Marattui  and  Angioptnis.  In  Dauini 
and  Kniil/iissi/i  it  is  simpler,  but  in  these  also  the  arrangement  of  the  bundles  in  the 
adult  stem  is  by  no  means  easy  to  trace.  A  thorough  study  of  the  condition  in  the 
early  stages  of  the  sporophyte  is  therefore  specially  important  for  understanding 
the  much  more  complex  arrangement  of  the  bundles  in  the  older  plant. 

In  view  of  the  conditions  that  we  have  found  to  exist  in  the  ( )phioglossace;e, 
and  particularly  the  nature  of  the  vascular  system  in  the  young  sporophyte  of 
Ophioglossiim  nioluccaniini,  a  careful  reinvestigation  of  the  developmental  history 
of  the  vascular  system  in  the  young  sporophyte  of  the  Marattiaceae,  especially  the 
simpler  and  presumably  more  primitive  genera  Dancta  and  Kaulfussia,  was  very 
much  needed.  To  this  end  series  of  sections  were  made  of  young  sporophytes  of 
both  of  the  latter  genera,  ranging  from  individuals  in  which  the  second  leaf  was 
still  undeveloped  to  those  in  which  a  dozen  or  more  leaves  had  been  formed.  These 
series  were  fairly  complete  and  made  it  possible  to  trace  quite  satisfactorily  the  evo- 
lution of  the  vascular  system  in  the  young  sporophyte  of  both  Dancra  and  Kaulfussia. 
Brebner  (Brebner  3)  has  given  an  accurate  account  of  the  distribution  of  the  bundles 
in  the  young  sporophyte  of  Damea  simplictfolia,  which  agrees  quite  closely  with  the 
arrangement  of  the  bundles  as  I  have  found  them  in  the  species  studied  by  me. 
Jeffrey  (  Jeffrey  3)  has  described  and  figured  a  few  specimens  of  D.  alata  (  .?),  but 
his  material  was  too  incomplete  to  make  the  study  at  all  satisfactory. 

The  available  material  of  Marattia  was  much  less  complete,  although  a  number 
of  stages  were  secured.  Farmer  has  made  an  exhaustive  study  of  the  vascular  system 
in  the  young  sporophyte  of  Angiopterts  (Farmer  3),  and  an  extended  study  of  Aii- 
giopteris  did  not  seem  necessary,  therefore,  except  for  a  study  of  the  early  stages  to 
determine  the  origin  of  the  vascular  bundles.  All  of  the  writers  mentioned  con- 
cerned themselves  almost  exclusively  with  the  fully  developed  bundles,  beginning 
their  study  at  the  base  of  the  stem  and  working  upward.  No  attempt  was  made  to 
follow  out  the  development  of  the  vascular  bundles  from  the  meristematic  region 
of  the  apex  and  proceeding  downward,- a  method  of  study  which  we  think  would 
have  materially  modified  the  conclusions  drawn  by  these  observers  in  regard  to  the 
relation  of  the  different  parts  of  the  vascular  system. 

In  my  studies  as  to  the  origin  of  the  vascular  system  in  the  young  sporophyte 
of  the  Marattiaceae  the  course  of  the  bundles  has  been  carefully  followed  in  series 
of  microtome  sections,  passing  downward  from  the  apical  meristem  to  the  base  of 
the  sporophyte,  where  the  axial  primary  bundle  passes  into  the  primary  root.  These 
series  of  transverse  sections  were  then  compared  carefully  with  series  of  longitudinal 
sections  of  young  plants  of  approximately  the  same  age,  and  in  this  way  a  clear 
conception  was  obtained  of  the  arrangement  of  the  vascular  system  within  the  stem 
of  the  young  sporophyte. 

THE  DEVELOPMENT  OF  THE  VASCULAR  SYSTEM  IN  DAN^,A. 

Especial  attention  has  been  given  to  the  development  of  the  vascular  system  in 
Dana-a  and  Kaulfussia,  as  these  have  received  less  attention  than  Marattia  and 
Angiopteris,  and  moreover  are  probably  more  primitive  forms  whose  structures  have 
departed  less  from  the  ancestral  type  than  those  of  either  Marattia  or  Angiopteris. 

A  longitudinal  section  of  the  young  sporophyte  of  Dancca  jamaicensis  at  the 
period  when  the  root  is  just  about  to  emerge  is  shown  in  fig.  I2i,  A.  The  root  in 
this  species,  as  in  D.  simplicifolia,  described  by  Brebner,  is  the  first  organ  to  appear 


161 


oiitsiik-  tin-  |ii(itlialliiim;  the  (.-()t\  Iidoii  ;it  this  time  is  still  very  small  ami  thi'  lamina 
is  scarcely  developed.  The  root  apex  does  not  show  in  the  section  figuied  and  all 
that  can  be  seen  is  the  upper  portion  of  its  stele,  which  joins  the  two  young  vascular 
bundles  that  extend  respectively  into  the  cotyledon  and  the  second  leaf,  which  can 
already  be  recognized.  The  greater  part  of  the  young  sporophyte  is  made  up  of 
large  thin-walled  cells.  Figure  I2i,  li,  shows  a  median  section  of  the  young  cotyledon 
from  this  same  embryo,  which  is  strongly  bent  over  the  stem  apex.  It  is  possible 
that  the  square  terminal  cell,  which  in  the  drawing  has  the  nucleus  indicated,  is  the 
apical  cell  of  the  leaf,  but  this  is  not  at  all  certain.  The  outer  part  of  the  cotyledon 
is  made  up  of  large  thin-walled  cells  like  those  which  compose  the  bulk  of  the 
sporophyte,  but  at  its  apex  there  is  active  cell  division,  and  traversing  the  young 
cotyledon  and  placed  somewhat  toward  its  inner  side,  can  be  seen  the  primary 
vascular  bundle,  made  up  of  elongated  procambium  cells.  This  bundle  can  be 
easily  followed  down  into  the  body  of  the  sporophyte,  where,  as  we  have  seen,  it  is 


sections  of  a  very  young  sporophyte  of  Danxa  jamaicensii.     ) 
A  shows  cotyledon  apex;  C,  apices  of  the  stem  and  second  leaf;  G  shows 


without  interruption  into  the  stek 


the 


lb 


ipex, 


which  does  not  show  in  the  figure,  is  in  a  slight  depression  close  tt)  the  base  of  the 
cotyledon  and  shows,  as  usual,  a  single  deep  apical  cell.  Nearly  opposite  the  cotyledon 
is  the  beginning  of  the  second  leaf  (/ ");  this  is  shown  in  median  section  in  fig.  121.  B. 
Ihe  group  of  narrow  columnar  cells  that  compose  its  apex  does  not  show  a  recog- 
nizable single  initial  cell.  A  short  distance  below  its  apex,  the  procambiimi  of  its 
vascular  bimdle  becomes  differentiated  and  is  continued  downward  until  it  joins 
the  bundle  from  the  cotyledon.  The  tissue  arising  above  the  junction  of  these  two 
bundles  and  continuing  upward  into  the  apex  of  the  stem  is  composed  of  absolutely 
undifferentiated  parenchyma  and  there  is  no  evidence  at  all  of  an\-  stelar  tissue  in 
the  stem  above  the  junction  of  these  two  primary  leaf  traces;  indeed,  the  stem  apex 
lies  decidedly  on  one  side  of  the  plane  which  traverses  the  vascular  bundles  of  the 
two  leaves.  Fig.  145  shows  a  number  of  cross-sections  from  a  series  taken  from  a 
large  embryo  of  Daneta  jamaicensis,  before  the  emergence  of  the  cotyledon  (//), 
11 


162 


THE    MARATTIALEt 


whose  apex  is  still  undivided.  C  shows  the  apices  of  the  stem  and  second  leaf,  the 
former  being  shown  on  a  larger  scale  in  G.  The  section  of  the  cotyledonary  bundle, 
lying  to  the  right  of  the  stem  apex,  is  plainly  evident  in  section  C.  D  shows  the 
separated  bundles  of  the  cotyledon  and  very  young  second  leaf,  which  lower  down 
unite  into  a  single  strand. 

Whether  we  can  properly  speak  of  a  stem  at  all  in  connection  with  the  tissues 
composing  the  central  region  of  the  young  sporophyte  is  questionable.  It  is  per- 
fectly evident  that  this  central  region  is  composed  partly  of  tissue  belonging  to  the 
base  of  the  cotyledon,  which  is  in  no  sense  to  be  looked  upon  as  an  adjunct  of  the 


-C.  Three  sections  near  the  stem  apex,  which  is  shown 
and  more  highly  magnified  in  D.    Fig.  C  is  revers 
position  with  reference  to  A. 
E.  The  central  region  of  C. 


F-J.   Show  the  condition  of  the  Vi 

region  of  the  sporophyte. 

H,  I.  Are  in  the  transition  region. 

J.  Shows  the  root  stele.    X200. 


stem,  and  partly  of  the  root  base;  the  two  structures,  i.  e.,  the  bases  of  the  root  and 
the  cotyledon,  merge  insensibly  into  each  other.  To  this  tissue,  derived  from  the 
root  and  the  cotyledon,  must  be  added  a  large  amount  of  superficial  tissue  derived 
originally  from  the  foot  of  the  embryo.  In  speaking  of  the  axis  of  the  young  sporo- 
phyte as  a  "stem"  it  must  therefore  be  borne  in  mind  that  this  stem  is  really  a 
composite  structure,  partly  leaf,  partly  root,  and  partly  foot. 

Fig-  ^3^y  ^  '>"<i  ^'  shows  two  longitudinal  sections  of  an  older  stage  after  the 
emergence  of  the  cotyledon.  A  passes  through  the  stem  apex  and  it  is  evident 
that  there  is  no  vascular  bundle  extending  into  the  stem.  The  tracheary  tissue  is 
now  well  developed  in  the  leaf  trace.  B  shows  the  trace  from  the  second  leaf 
at  its  point  of  junction  with  the  bundle  from  the  cotyledon.    In  fig.  138,  C  is  a  similar 


Till-    OLDKR    SI'OROPH^rr.  153 

stasif  to  ihat  shown  in  ./,  hut  tut  at  rit^lit  angles  to  it,  so  as  to  sliow  tlic  continuity 
oftliL-  Inuullcs  ot  the  cotyledon  and  ]m  imary  root,  which  together  constitute  the  prinia- 
ly  axial  vascular  bundle  of  the  sporophyte,  as  they  do  in  Op/iioglossum  nioluccaiuitii. 
ihe  similarity  of  such  a  section  as  that  figured  to  the  similar  stage  in  O.  rnoliirr/uiimi 
is  suHicicntly  obvious.  The  stem  apex  is  shown  in  fig.  140,  .7,  and  the  lutliment  of 
the  second  leaf  is  shown  in  fig.  140,  B. 

F'igure  146  shows  ten  transverse  sections  from  a  series  made  from  a  young  sporo- 
phyte ofi).  jainaiccnsis  of  almost  exactly  the  same  age  as  that  shown  in  fig.  138,  B. 
A  is  cut  above  the  level  of  the  stem  apex  and  passes  through  the  cotyledon  and  apex 
of  the  second  leaf.  The  arrangement  of  the  cells  at  the  apex  of  the  latter  suggests 
the  possibility  of  a  single  apical  cell.  The  base  of  the  petiole  of  the  cotyledon  is 
much  flattened  and  is  made  up  of  large,  thin-w^illed  parenchyma  with  no  traces  of 
tannin  cells  or  mucilage  ducts.  The  vascular  bundle  is  oval  in  outline  and  decidedly 
collateral  in  structure.  There  is  no  recognizable  endodermis,  and  I  shall  not 
attempt  to  say  whether  the  cells  immediately  surrounding  the  bundle  should  be 
spoken  of  as  endodermis  or  pericycle.  Except  for  two  small  tracheids  on  the  inner 
side  of  the  bundle  the  vascular  bundle  is  composed  of  delicate  tissue,  apparently 
parenchyma,  but  some  of  the  larger  elements  undoubtedly  represent  sieve  tubes. 
Brebner  states  that  the  sieve  tubes  in  D.  stmplicifolia  (Brebner  3,  page  524)  do  not 
show  clearly  in  sections  mounted  in  Canada  balsam,  but  when  examined  in  other 
media  they  show  thick,  glistening  walls  and  pitted  areas.  This  point  was  not  further 
examined  in  the  species  under  consideration,  but  would  probably  agree  with  the 
observations  made  by  Brebner  upon  D.  simplicifolia. 

Section  B  passes  through  the  stem  apex,  whose  apical  cell  is  shown  on  a  larger 
scale  in  D.  The  cotyledon  trace  in  this  section  shows  three  tracheids.  In  D  the 
section  is  made  a  short  distance  below  the  stem  apex  and  shows  the  second  leaf  trace 
bending  in  to  join  the  trace  from  the  cotyledon.  The  central  part  of  the  section  is 
shown  more  enlarged  in  E,  and  it  is  perfectly  clear  that  the  region  immediately 
below  the  apex  and  lying  between  two  leaf  bases  shows  nothing  which  can  be 
interpreted  as  a  cauline  stele.  F  and  G  show  sections  taken  still  further  down, 
illustrating  the  coalescence  of  the  two  leaf  traces  to  form  the  single  axial  stele.  In 
G  there  is  seen  the  first  tracheid  belonging  to  the  leaf  trace  from  the  second  leaf, 
and  in  H  the  central  bundle  is  complete  and  there  are  seen  the  two  xylem  masses 
corresponding  respectively  to  the  two  leaf  traces.  One  of  these,  belonging  to  the 
primary  leaf  trace,  is  more  developed  than  the  other  one.  The  larger  xylem  mass 
in  this  case  had  five  tracheids  and  the  smaller  one  three.  /  and  /  are  transitional 
stages  between  the  bundle  of  the  cotyledon  and  the  root,  and,  proceeding  down- 
ward, the  bundle  becomes  somewhat  smaller  and  there  is  a  reduction  in  the  number 
of  tracheids,  which,  however,  are  plainly  seen  to  be  continuous  in  their  development 
with  the  two  .xylem  masses  in  the  central  bundle  of  the  stem,  formed  by  the  junction 
of  the  two  primary  leaf  traces,  which  maintain  their  identity  until  they  merge  into 
the  two  xylem  masses  of  the  diarch  root.  Within  the  root  itself  the  endodermis 
surrounding  the  bundle  is  very  conspicuous.  The  cells  making  up  the  endodermis 
are  of  large  si/e  and  the  characteristic  markings  upon  their  radial  walls  are  very 
easily  .seen.  The  limits  of  the  endodermis  become  much  less  clear  in  the  transi- 
tional region,  and  higher  up  it  is  difficult  to  make  out  a  clearly  defined  endodermis. 
Brebner  figures  a  very  irregular  endodermis  in  the  stem  of  D.  siriipliiifolia,  and 
perhaps  we  may  assume  that  a  proper  endodermis  is  present  also  in  the  young  stem 
of  D.  jamatccnsis,  but  it  is  certainly  very  inconspicuous,  to  say  the  least,  in  the  central 
region  of  the  young  sporophyte,  in  strong  contrast  to  the  very  conspicuous  endo- 
dermis in  the  root.    Farmer  (Farmer  3)  was  able  by  treatment  with  sulphuric  acid 


164 


THE    MARATTIALES 


to  demonstrate  an  external  endoderniis  in  the  stem  bundles  oi Angiopteris,  Marattia, 
and  Kaiilfussia,  and  presumably  similar  treatment  would  show  its  presence  in  the 
young  s  em  of  Daiicea. 

It  is  evident  that  we  can  not  speak  of  the  young  sporophyte  in  Dancea  jamai- 
censis  as  possessing  in  its  early  stage  a  "protostele,"  or  "haplostele,"  to  use  Brebner's 
terminology,  unless  we  choose  to  call  the  single  leaf  trace  of  the  cotyledon  a  protostele. 
Just  so  soon  as  the  two  first  leaf  traces  unite,  the  axial  vascular  bundle  of  the  young 
sporophyte  has  two  quite  independent  xylems. 

Figure  147  is  a  longitudinal  section  of  a  sporophyte  of  D.  cUiptica,  slightly 
older  than  that  of  D.  jamaicensis  shown  in  fig.  138.  The  second  leaf  (/^)  had  already 
begun  to  develop  the  lamina,  whose  apex  was  forked  so  that  there  were  two  veins 
present.  A  longitudinal  section  of  one  of  the  two  leaf  lobes  is  shown  in  D.  The 
stem  apex  closely  resembles  that  of  D.  jamaicensis,  the  apical  cell  having  much  the 
same  form  and  size.    The  stem  apex  does  not  lie  in  the  same  plane  as  the  leaf  traces 


A.  Nearly  medi 

origin  of  second 

B.  Central  region.     > 


¥u,.  n-j.—  Dait^a  elliptii 
section  of  a  young  sporophyte,  showing 


C.  Median  section  of  second  leaf. 

D.  Apex  of  second  leaf.     X150. 

E.  Stem  apex.      X150. 


and  hence  does  not  show  in  the  figure,  which  is  a  section  passing  directly  through 
the  leaf  traces.  This  plant  showed  very  clearly  the  very  earliest  stage  of  the  second 
root  (fig.  147,//,  r).  The  apical  cell  of  the  young  root  is  cut  out  from  one  of  the  cells 
of  the  parenchyma  below  the  stem  apex,  lying  almost  exactly  half-way  between  the 
two  primary  leaf  traces.  Only  a  single  segment  had  been  cut  off  from  the  apical 
cell  in  this  case  and  both  the  apical  cell  and  this  primary  segment  were  easily  dis- 
tinguished from  the  surrounding  tissue  by  their  denser  contents.  There  is  nothing 
to  indicate  that  the  cell  which  had  assumed  the  function  of  the  root  initial  was  in 
any  way  essentially  different  from  the  neighboring  cells.  If  it  is  an  endodermal  cell 
there  is  no  way  of  recognizing  this,  as  the  endoderniis  could  not  be  recognized  in 
this  part  of  the  sporophyte.  Figure  147,  B,  shows  an  enlarged  view  of  this  young 
root  initial,  lying  above  the  junction  of  the  two  primary  leaf  traces.  Conspicuous 
reticulate  tracheids  with  pointed  ends  are  present  in  the  trace  from  the  cotyledon, 
but  as  yet  no  permanent  tissue  has  been  developed  in  the  bundle  from  the  second  leaf. 


THE    OI.nr-R    SPOROPHYTE  165 

A  somewhat  older  spoiophyte  from  D.  janiaicensis  is  shown  in  fig.  148.  In 
this  plant  the  third  leaf  was  plainly  visible  and  the  second  root  had  developed  into 
a  short  conical  body  which  was  pushing  its  way  through  the  tissues  between  the 


insertion  of  the  first  and  second  leaves.  By  this  time  tracheary  tissue  haS  developed 
in  the  bundle  from  the  second  leaf,  and  now  for  the  first  time  we  note  the  presence 
of  large  tannin  cells  in  the  neighborhood  of  the  vascular  bundles.  Three  of  these 
are  shown  in  fig.  149,  lying  next  the  bundle  of  the  second  leaf.     The  irregular  ring 


of  the  sporophyte  shown  in  fiq.  148. 


of  narrow  cells  shown  in  the-  figure  and  hing 
point  of  insertion  of  the  second  root.  Figure 
of  the  apex  of  this  second  root.     'I"he  apical 


below  tile  a]iical  meiistem  marks  the 
149,  /i,  shows  a  nearh'  median  section 
cell  is  nearly  oblong  in  form  and  the 


lateral  segments  are  very  large  and  periclinal  segments  which  contribute  to  the  root 


166 


THE    MARATTIALES 


cap  are  cut  off  from  them.  The  outer  cells  of  the  root  cap  are  very  much  enlarged 
and  there  is  an  evident  space  between  the  root  and  the  surrounding  tissues.  The 
trace  from  the  third  leaf  joins  that  of  the  second  one  close  to  its  union  with  the 
bundle  from  the  cotyledon  (fig.  148,  B). 

In  fig.  150  are  shown  nine  cross-sections  from  a  series  made  from  a  plant  of  D. 
jamaicensis,  in  which  four  leaves  were  evident.  A  microscopic  examination  ot  the 
stem  apex  showed,  however,  that  a  fifth  leaf  was  also  present,  which  stood  nearly 
directly  opposite  the  cotyledon.  A  shows  sections  only  of  leaves  3  and  4,  the  latter 
having  the  stipules  conspicuous,  while  these  are  absent  or  scarcely  developed  at  all 
on  the  first  three  leaves,  at  least  in  the  specimen  in  question.  Between  the  leaves 
are  seen  sections  of  the  numerous  scales  which  beset  the  surface  of  the  young  leaves. 
B  is  taken  somewhat  lower  down  and  includes  a  section  of  leaf  5.  C  passes  through 
the  stem  apex  and  shows  clearly  the  spiral  arrangements  of  the  first  five  leaves, 
each  of  which  has  in  its  petiole  a  single  concentric  bundle  which  becomes  larger  in 


ig  sporophyte,  with  t1 
apex.    Roman  figures 


D.  jamaicensis. 

fully-developed  leaves  and  two  younger  t 


each  successive  leaf,  with  a  corresponding  increase  in  the  development  of  the  xylem. 
As  the  sections  are  examined,  farther  and  farther  down  in  the  stem  {D  to  F),  one 
can  see  very  clearly  the  way  in  which  the  single  bundle  in  the  lower  part  of  the 
stem  owes  its  origin  to  the  coalescence  of  the  leaf  traces.  Proceeding  downward 
the  traces  of  leaves  4  and  5  are  seen  to  approach  gradually  and  finally  to  become 
completely  coalescent;  and  still  further  down  {F)  the  leaf  trace  from  3  joins  that 
from  4,  and  a  single  bundle  results,  crescent-form  in  section,  but  showing  ckarl\  its 
compound  nature.    1  he  three  xylems  never  become  entirely  confluent. 


THE    OLDKR 


167 


For  a  long  time  sections  of  the  stem  show  this  single  central  Inmclle  of  crescentic 
form,  at  Hrst  tleiived  from  the  coalescence  of  the  third,  fourth,  and  Hfth  leaf  traces, 
but  continued  upward  in  the  same  form  and  added  to  by  the  addition  of  the  traces 
from  the  subsequent  leaves.  I'his  crescentic  stele,  which,  for  convenience  may 
be  spoken  of  as  the  stele  of  the  stem,  is  entirely  of  foliar  origin.  The  crescent  never 
becomes  completely  closed  and  its  opening  in  the  earlier  stages  of  development  can 
not  be  properly  called  a  foliar  gap.  The  parenchyma  which  is  inclosed  within  its 
curve  belongs  from  the  first  to  the  ground  tissue  and  is  not  part  of  the  stele.  Some 
of  the  surrounding  cells  show  traces  of  the  typical  endodermal  markings  and  it  is 
perhaps  safe  to  say  that  the  stele  is  bounded  by  an  endodermis,  as  Farmer  states  is 
the  case  in  Angtopteris  and  Brebner  in  D.  simplicifolia.  The  limits  of  the  endo- 
dermis, however,  especially  upon  the  concave  side  of  the  stele,  are  very  vague.  The 
stele,  after  the  complete  fusion  of  the  three  leaf  traces,  may  perhaps  best  be  described 


Fig.  151. 


Four  longitudinal  sectic 


rth  leaf,  /*,  has  the  stipules  well  dc 


as  concentric  in  structure,  with  phloem  developed  all  around  the  xylem,  but  there 
are  probably  traces  of  phloem  also  between  the  three  xylems  which  represent  the 
three  confluent  leaf  traces. 

In  the  older  portions  of  the  stem  the  bundles  become  still  more  completely 
fused  and  the  compound  bundle  is  oval  in  outline,  but  still  shows  plainlv  the  three 
xylems  of  its  constituent  leaf  traces  (fig.  150,  G).  In  this  region  the  endodermis 
is  rather  better  developed  than  it  is  higher  up,  but  its  limits  are  still  rather  vague. 
At  this  level  the  traces  of  the  leaves,  i  and  2,  are  still  free,  but  have  approached 
nearer  to  the  central  bundle  than  is  the  case  higher  up. 

Still  lower  down,  the  trace  from  the  second  leaf  joins  the  Iniiulle  formed  from 


the  later  leaf  traces, 
proaches  the  conditi 
using  Brebner's  teir 


which  no  longer  clearly  shows  the  sepa: 
11  whiili  has  been  desciilnd  as  "  pi dtusleli 
iin()li)"\-.       I  he  wiem  tknunts.  liu\\i\ei. 


but 

osteli 


168 


THE    MARATTIALES 


core,  but  are  more  or  less  scattered,  with  thin-walled  elements  between.  After 
fusion  of  the  second  leaf  trace  with  this  is  complete,  the  section  of  the  stem  shows 
only  two  bundles,  representing  the  two  first  leaf  traces,  and  finally  (fig.  150,  H  and  /) 
the  section  of  the  stem  shows  the  condition  already  described  for  the  sporophyte 
with  but  two  leaves.  These  finally  merge  into  a  single  primary  axial  bundle  (/), 
which,  followed  downward,  merges  imperceptibly  into  the  stele  of  the  primary  root. 
Near  the  middle  of  these  lower  sections  can  be  seen  a  section  of  the  second  root, 
which  pursues  a  downward  course  through  the  cortical  tissue  for  a  very  long  distance, 
but  finally  emerges  and  grows  downward,  side  by  side  with  the  primary  root.  The 
third  root  (fig.  150,  G,  r")  emerges  much  higher  up  and  breaks  through  the  cortex 
at  about  the  level  of  the  junction  of  the  three  youngest  leaf  traces. 

Fig.  153  shows  the  details  of  the  central  tissue  from  the  same  sporophyte  as 
that  just  described.  J  passes  through  the  stem  apex  and  shows  the  apical  cell  cut 
somewhat  obliquely,  and  near  it  the  section  of  the  trace  from  the  fifth  leaf.  D  is  z 
section  of  the  fourth  leaf  trace  from  the  same  level.  This  shows  but  two  tracheids 
at  a  point  near  the  inner  limits  of  the  bundle,  while  on  the  outer  side  there  is  a  con- 
spicuous curved  line  of  protophloem  cells.  5  is  a  section  taken  somewhat  lower 
down  and  shows  the  bending  in  of  the  leaf  trace  as  it  descends  into  the  stem.  This 
is  still  more  marked  in  the  fifth  leaf  trace,  which,  at  this  level,  has  a  crescentic  form, 


A.  Apex  of  fifth  leaf  from  sporophyte  shown  in  fig. 

B.  Stem  apex  of  same. 

C.  Base  of  third  root,  showing  triarch  bundle  and  r 


but  no  permanent  elements  yet  developed.  It  is  probable  that  a  portion  of  this 
crescentic  mass  of  procambium  represents  the  sixth  leaf  trace.  The  fourth  leaf 
trace  at  this  point  shows  three  tracheids  which  are  decidedly  larger  than  those 
higher  up,  and  still  lower  down  the  tracheids  increase  still  more  in  size  and  several 
tannin  cells  can  be  seen  in  contact  with  them.  The  section  of  the  fourth  leaf  trace 
is  connected  with  the  large  but  undifferentiated  trace  of  the  fifth  leaf  by  an  isthmus  of 
procambium  cells,  so  that  the  sections  f)f  the  two  bundles  form  the  crescent-shaped 
section,  similar  to  that  seen  lower  down  (fig.  153,  C).  The  tracheary  elements  of  the 
fused  portion  of  the  fourth  leaf  trace  are  noticeably  larger  again  than  those  in  the 
free  portion  of  the  leaf  trace.  We  now  notice,  for  the  first  time,  traces  of  the  mucilage 
ducts  which  afterwards  become  so  conspicuous  in  the  stem.  These  first  appear  in 
section  as  rounded  cells  (m),  and  it  is  evident,  as  Farmer  has  shown  in  Arigiopteris, 
that  the  earliest  mucilage  canals  are  of  lysigenous  origin,  i.  e.,  they  are  formed  by  a 


169 


fusion  of  ctlls  and   not 


splirtinii  apa 
ibout  this  intercellular  spac 


)t"  the-  (.(.lis  and  tin-  dcvilopnicnt  of" 
In  liis  taiiicr  paper  Hrehner  states 
that  the  mucilage  ducts  are  schizogenous,  but  in  his  later  paper  he  admits  that  they 
may  he  of  lysigenous  oiigin,  which  certainly  is  the  case  in  the  species  of  Datia'a 
described  here. 

Ihe  details  of  the  older  central  bundles  of  the  sections  /•  and  (/',  Hg.  150,  are 
shown  in  fig.  153,  E,  F:  the  shaded  cells  in  6'  are  tannin  cells. 

Figure  151  shows  longitudinal  sections  of  a  young  sporophyte  of  /^.  elltptica, 
of  about  the  same  age  as  the  sporophyte  which  has  just  been  described.  This  al.so 
shows  three  fully  developed  leaves,  while  the  fourth  and  fifth  leaves  are  well  advanced. 


-Ql^i    P 


153.— Details  of  th< 


lar  system  of  sporophyte  : 


A.  Passes  through  the  stem  apex;  B  and  C,  lower  down 
D.  A  single  leaf  trace.  X150.  E,  F.  Vascular  bundles  frc 


,mfig..50 
showing  the  fourth  and  fifth  le; 
1  the  lower  part  of  the  stem,  m,  h 


young  mucilage  ducts 


The  central  bundle  of  the  stem  formed  by  the  junction  of  the  three  first  leaf  traces 
is  now  conspicuous  and  forms  a  stout  central  strand,  continuing  downward  into  the 
primary  root  (;').  //  is  a  nearly  median  section,  passing  through  the  stem  ape.x, 
whose  large  and  conspicuous  apical  cell  is  shown  in  fig.  152,  B.  The  ape.\  of  the 
fifth  leaf  is  seen  just  above  this  and  a  more  enlarged  figure  of  this  is  shown  in  fig. 
152,  A.  The  apex  of  the  fifth  leaf  (which  is  here  cut  transversely)  is  occupied  bv  a 
small  group  of  large  cells,  of  which  the  central  one  may  perhaps  represent  a  single 
initial  cell.  Below  the  stem  apex,  but  separated  from  it  by  a  considerable  amount 
of  tissue,  can  be  seen  the  bases  of  the  leaf  traces  from  the  fourth  and  fifth  leaves 
respectively.      These  are  joining  the  central   bundle  of  the  stem   near  the   junction 


170 


THE    MARATTIALES 


of  the  third  leaf  trace,  and  at  this  point  there  may  be  seen  the  base  of  the  third  root 
(r").  Between  the  fourth  and  fifth  leaf  traces  is  present  a  section  of  the  first  mucilage 
duct.  5  is  a  section  some  distance  to  one  side  of  the  apex,  also  passing  through  the 
primary  mucilage  canal  and  the  fourth  root,  which  arises  between  the  fourth  and 
fifth  leaf  traces.  Figures  C  and  D  are  sections  on  opposite  sides  of  the  stem  apex 
from  B.  The  fourth  leaf,  with  its  conspicuous  stipules  (st),  showsjn  these  sections, 
and  the  third  root  can  also  be  seen.  Fig.  152,  C,  is  a  more  enlarged  view  of  the 
third  root  shown  in  fig.  151,  D.  The  root  is  triarch  and  in  the  peripheral  part  of  the 
cortex  there  is  visible  a  row  of  very  conspicuous  cells  whose  walls  stain  very  strongly 
with  safranine  and  in  section  closely  resemble  large  tracheary  elements.  A  longitudinal 
section  of  these  cells,  which  are  also  conspicuous  in  the  later  roots  (fig.  155),  shows 
that  they  are  elongated  sclerenchyma  cells  whose  thick  walls  are  conspicuously 
pitted.     Farmer  (Farmer  3)  observed  similar  cells  in  the  roots  of  Jngiopteris. 


Figures  154  and  155  show  three  longitudinal  sections  of  a  pretty  well  advanced 
young  sporophyte  of  D.  jenmatii.  The  root  (shown  in  the  figure  emerging  at  the 
base)  is  probably  the  second  root.  The  stem  has  already  begun  to  assume  a  dorsi- 
ventral  form,  and  the  basal  part  of  the  root,  which  is  strongly  cui-ved,  is  cut  away 
and  so  does  not  show  in  these  sections.  The  earliest  leaves  are  no  longer  recognizable 
and  it  is  impossible  to  determine  just  how  many  leaves  have  been  formed.  The 
leaves  first  formed  have  the  single  trace  characteristic  of  the  first  leaves  in  all  of 
the  species,  but  the  youngest  leaves  show  that  the  leaf  trace  is  double.  In  this  sec- 
tion (fig.  155,  A)  is  shown  a  very  young  leaf,  cut  through  parallel  to  its  surface 
and  showing  clearly  the  stipules  at  its  base  and  also  the  young  vascular  bundles. 
Within  the  leaf  are  two  bundles,  which  are  seen  to  join  at  its  base,  but  separate 
again  lower  down,  the  two  bundles  thus  forming  two  distinct  traces  in  the  stem.  In 
fig.  154,  B,  the  section  passes  through  the  youngest  root,  which  is  seen  to  have  its 
stele  joined  to  one  of  the  leaf  traces  from  the  youngest  leaf.  Several  conspicuous 
mucilage  ducts  are  now  present  in  the  stem  near  the  vascular  bundles;    these  are 


THE    OLDER    SPOROPHYTE 


171 


formed  of  rows  of  large  cells  which  become  more  or  less  fused  tf)gether  and  their 
contents,  composed  of  a  dense  granular  mucilage,  stain  very  strongly,  either  with 
safranine  or  with  IJismarck  brown,  which  were  the  principal  stains  used  in  preparing 
the  sections.  Numerous  tannin  cells  are  also  present,  scatrcncl  irregulari\- through 
the  cortical  tissue  and  also  in  the  vascular  bundles. 

Figure  155,  B,  is  a  median  section  through  the  base  of  one  of  the  later  roots, 
showing  its  connection  with  the  corresponding  bundle  in  the  stem.  The  elongated 
cells  {sc)  are  the  cortical  sclerenchyma  cells  already  referred  to.  These  are  shown 
on  a  larger  scale  in  C  and  D,  where  the  conspicuous  pitted  walls  can  be  seen. 
The  shaded  cells  in  the  figure  are  tannin  ceils. 

Figure  156  shows  cros.s-sections  taken  at  different  heights  from  a  sporophyte  of 
D.jenmani,  a  plant  of  about  the  same  age  as  that  which  was  shown  in  the  preceding 
series  of  longitudinal  sections.     Sections  made  near  the  apical  region,  A,  B,  and  C, 


A.  Another  section  of  specimen  siiown  in  fig.  154. 

B.  Base  of  a  root  showing  sclerenchyma,  sc,  in  cor 

C.  Sclerenchyma  cells,  showing  pitted  walls.     X5: 

D.  Surface  view,  showing  pits. 


show  two  pretty  well  advanced  leaves  and  the  first  trace  of  a  third,  the  apex  of  which 
is  indicated  in  C  and  E.  Unlike  the  earlier  leaves  with  their  single  leaf  tiace,  these 
later  leaves,  as  we  have  seen,  have  the  petiole  traversed  by  two  vascular  bundles 
whose  sections  are  plainly  visible.  These,  as  we  have  remarked  from  a  study  of  the 
longitudinal  sections,  fuse  into  one  near  the  base  of  the  leaf  (//),  and  two  small 
bundles  are  also  present  on  either  side,  belonging  to  the  stipules.  As  the  sections 
are  followed  downward,  the  main  bundle  is  found  to  divide  into  the  double  leaf  trace 
entering  the  stem,  and  the  two  small  stipide  bimdles  become  uniteil  with  these,  so 
that  within  the  stem,  at  about  the  level  of  the  stem  ape.x,  two  distinct  bundles  are 
seen,  corresponding  to  each  leaf.  Ihe  leaves  are  now  arranged  in  two  series, 
indicating  that  the  dorsiventral  character  of  the  stem  in  this  species  is  established 
and  the  youngest  leaf  lies  almost  opposite  the  next  xoungest  oni\  whose  leaf  traces 
can  be  seen.  E  shows  the  stem  :i]iex  with  the  apical  cell.  \.  ami  the  \(umgest  leaf 
rudiment,  /. 


172 


THE    MARATTIALES 


Below  the  level  of  the  stem  apex,  the  stele  of  the  axis  closely  resembles  that 
already  described  from  the  somewhat  younger  plant  and  forms  a  somewhat  irregular 
crescent,  evidently  composed  of  two  portions  which  are  joined  on  the  side  facing  the 
two  leaf  traces  from  the  oldest  leaf  which  shows  in  this  section.  The  opening  of  the 
crescent  at  this  level  is  turned  away  from  the  leaf.  No  permanent  elements  are 
present  in  the  central  stele  as  yet.  Following  this  downward,  the  crescent  is  seen 
to  open  on  the  side  next  the  two  oldest  leaf  traces  and  there  is  thus  formed  a  foliar 
gap,  while  on  the  opposite  side  the  space  becomes  closed.  In  section  D,  which 
is  taken  lower  down,  the  position  of  the  section  of  the  central  stele  is  reversed.     At 


A-D.  Four  transverse  sections  of  a  young  sporophyt 

E.  The  apical  meristem  with  apical  cell  of  stem, 

F-I.  Four  sections  from  the  same  series,  but  taken 

stele.     »;,  mucilage  ducts.     Between  the  i 


•  oi  D.jenmani.     X20.    Section  C  shows  stei 
r,  and  a  leaf  initial, /.     X180. 
lower  down.    X20.    Figs.  F,  G,  show  fusion 
lucilage  ducts  in  G  can  be  seen  the  small  i 


this  point  the  section  of  the  central  stele  forms  a  crescent  ot  tissue,  most  of  which 
has  not  passed  beyond  the  procambial  stage.  This  crescent-shaped  mass  is  evi- 
dently composed  of  two  parts  and  represents  mamly  the  basal  undivided  bundles 
of  the  two  youngest  leaves.  Tracheary  tissue  has  begun  to  develop  in  the  older  of 
these  two  masses.  Occupying  the  space  within  this  crescentic  stele  are  three  young 
mucilage  canals,  but  none  are  yet  developed  in  the  cortical  tissue  of  the  stem. 
Within  this  central  space  there  can  also  be  seen  the  section  of  a  small  isolated  group 


THK    OLDKR    SI'OKOrinTr, 


173 


;i\lal  stele  in  loiiimissural  j 
itii  Hvc  leaves.  The  older  k 
Ininclle,  e-resceiit-shaped  in 


laiul  whuh  hac 
t  base,  shown  ii 
iLitlinc  and  eon 
bundles  belong 


of  procanibial  cells.      This  is  the  singk'  axial  stele  oi   eonmiissural  strand  which  had 

not  yet  begun  to  develop  in  the  plant  \ 

this  section,  has  a  single  large  vascula 

centric  in  structure,  and  there  are  also  seen  the  two  small  concentru 

ing  to  the  stipules. 

All  the  leaf  traces  in  the  older  leaves  are  concentric  in  structure,  with  well- 
developed  internal  phloem,  and  thus  differ  from  the  collateral  traces  of  the  earliest 
leaves.  This  concentric  structure  of  the  bundle  is  already  well  marked  in  the  fourth 
leaf,  where,  however,  the  protophloem  is  mainly  developed  upon  the  outer  side.  /• 
shows  the  arrangement  of  the  bundles  in  a  section  somewhat  further  down.  I  he 
two  strands  from  the  oldest  of  the  three  leaves  seen  in  the  apex  have  joined  the  horns 
of  the  crescentic  central  bundle,  which  still  shows  clearly  its  dual  nature.  In  the 
younger  of  the  two  portions  of  these  sections  the  first  tracheids  have  just  appeared 
near  the  free  end,  while  in  the  older  half  a  line  of  tracheids  extends  nearly  through 
the  whole  of  the  center.  The  mucilage  ducts  at  this  level  are  much  larger  and  their 
cells  have  become  confluent.     Close  to  the  large  mucilage  canal  can  be  seen  the 


A 

Fig.  157. 

A.  Section  of  an  older  stem  of  Danaa  jenmaitiy  showing  cortical  iniicilaj;c  ducts,  w,  and  tcntral  or 
,  commissural  strand,  c.    //,  leaf  trace,    r,  root.     X20. 

B.  Shows  a  section  higher  up,  with  free  leaf  traces  and  commissural  strand. 

section  of  the  axial  vascular  strand,  which  somewhat  higher  up  turns  outward  and 
becomes  fused  with  the  inner  face  of  the  crescentic  central  stele.  The  leaf  traces 
soon  become  completely  merged  with  the  broad  crescentic  stele  and  their  limits 
can  no  longer  be  recognized.  The  foliar  gap  gradually  closes  up  and  the  two  por- 
tions of  the  crescent  separate  at  a  point  opposite  so  as  to  form  a  leaf  gap,  nearly- 
opposite  the  first  one;  but  I  have  seen  no  cases  where  a  section  of  the  central  stele 
appears  as  an  unbroken  ring,  although  it  is  possible  that  this  might  occur  for  a 
brief  period.  Much  the  same  condition  of  things  is  seen  lower  down  and  it  is  clear 
that  in  all  cases,  after  the  double  leaf  trace  has  been  developed,  one  bundle  fuses 
with  an  older  and  one  with  a  younger  leaf  trace.  The  axial  bundle  shows  a  central 
mass  of  tracheary  tissue,  and  in  somewhat  older  stages  an  endodermis  is  pretty  well 
developed.  Finally  this  bundle  can  be  traced  downward  to  where  it  connects  with 
the  main  stele,  composed  of  the  united  leaf  traces.  The  main  stele  gradually  passes 
down  into  the  base  of  the  stem,  where  it  shows  the  structure  already  described  for 
the  younger  sporophyte. 

In  older  sporophytes  the  crescentic  central  stele  becomes  brokt  n  up  perniaiu  iul\ 
into  two  elongated  masses  when  seen  in  section  (fig.  157),  but  the  junction  of  the 


174 


THE    MARAITIALES 


leaf  traces  with  these  takes  phice  exactly  as  in  the  younger  plant.  Fig.  157,  B,  shows 
the  separate  leaf  traces  and  the  free  axial  strand,  while  in  A  the  leaf  traces  are 
becoming  fused  with  the  broad  central  strands  and  the  axial  strand  is  also  anastomos- 
ing with  one  of  the  latter.  This  has  taken  place  at  the  point  of  junction  with  a 
root.  While  in  the  younger  sporophyte  the  mucilage  ducts  are  confined  to  the  central 
region,  in  the  older  plant  they  occur  also  in  the  peripheral  region  of  the  stem  (fig. 
157,  >n).    The  details  of  the  vascular  bundles  are  shown  in  figs.  158  and  159. 


To  recapitulate:  The  vascular  system  in  the  young  sporophyte  of  Daiura 
begins  as  a  single  axial  strand,  which  is  continuous  through  the  cotyledon  and  root. 
At  a  very  early  period  a  second  vascular  bundle  or  stele  is  formed  in  the  second  leaf 
connecting  with  the  primary  strand,  and  this  is  followed  by  a  similar  single  strand 
or  stele  in  each  succeeding  leaf,  up  to  about  the  seventh.  Up  to  this  time,  except 
for  the  steles  of  the  secondary  roots,  the  whole  vascular  system  is  built  up  of  united 


leaf  traces  and  there  is  no  cauline  bundle  in  the  strict  sense  of  the  word,  although 
we  may  speak  of  the  bundle,  or  stele  of  the  stem,  as  soon  as  there  is  a  solid  central 
strand  formed  below  the  junction  of  the  earlier  leaf  traces.  This  primary  stele 
never  has  the  form  of  a  true  protostele,  however,  as  the  xylems  belonging  to  the 
separate  leaf  traces  can  be  recognized  and  the  compound  nature  of  this  central 
bundle  is  unmistakable. 


TIIK    OLDKK    Sl'OKOl'H'lTl'  175 

At  a  later  stage-,  piohablv  about  the  time  that  the  seventli  leaf  is  toinieii,  theie 
arises  the  single  axial  (coiiiniissuial)  stiaiul.  which  is  caiiline  in  its  oiigiii  aiul  which, 
as  lirebner  has  stated  foi-  D.  snti/>licifalia,  is  the  only  strictly  caiiline  portion  of  the 
vascular  system  ot  the  stem.  Ihis  can  first  be  seen  at  about  the  same  time  that  the 
tlrst  double  leaf  trace  appears. 

The  development  of  the  vascular  system  was  not  traced  fuither,  as  it  has  already- 
been  adequately  described  by  Kiihn  ( Kiihn  2),  and  except  tor  the  increased  number 
of  leaf  trace  and  commissural  strands  the  vascular  system  is  essentially  the  same 
in  a  young  plant  like  that  shown  in  fig.  157  as  it  is  in  the  adult  sporophyte. 

Brebner's  account  of  the  development  of  the  young  sporophyte  in  Dan, in 
simplicifolia  agrees  essentially  with  my  own  studies  of  D.  eUiptica,  D.  jetmnnii,  and 
D.  jamaicensts.  He  failed,  however,  to  get  successful  sections  of  the  transition 
region  between  the  root  and  the  cotyledon,  or,  as  he  puts  it,  "between  the  root  and 
stem,"  and  his  statements  that  the  central  bundle  begins  as  a  "haplostele,"  i.  e., 
a  protostele,  is  not  borne  out  by  my  studies  on  the  other  species.  Moreover,  his 
statement  that  "in  this  way  the  somewhat  irregular  adelosiphonic  dictyostele  of 
Dantra  is  established  now  by  a  process  which  is,  to  all  intents  and  purposes,  a 
branching  of  the  haplostele,  due  to  the  departure  of  the  leaf  traces  of  closely  set, 
spirally  arranged  leaves,"  might  better  be  stated,  "the  dictyostele  arises  by  a  process 
which  is  essentially  the  fusion  of  the  leaf  traces  of  closely  set,  not  necessarily  spirally- 
arranged  leaves."  He  fully  recognized  the  important  part  which  the  leaf  traces 
play  in  the  building  up  of  the  dictyostele  of  the  stem,  but  he  did  not  apparently 
recognize  these  as  the  sole  factors  in  the  development  of  the  dictyostele  of  the  older 
stem.  He  does,^however,  specifically  state  that  the  axial  t)r  commissural  strand  is 
the  only  part  of  the  vascular  system  which  is  strictly  of  cauline  origin. 

THI<;  ADULT  Sl^OROPHYTE  OF  DAN.ilA. 
The  anatomy  of  what  was  supposed  to  be  the  sporophyte  of  Dancea  was  first 
described  by  Holle  (Holle  2),  but  the  later  investigations  of  Kiihn  showed  that  the 
plant  investigated  by  Holle  could  not  have  been  a  Dancea,  nor  could  it  even  have 
belonged  to  the  Marattiaceae,  since  Holle  describes  the  rhizome  as  developing  a 
sheath  of  sclerenchyma,  a  condition  of  things  which  has  not  been  found  to  exist 
in  any  Marattiaceae.  Kiihn's  account  is  very  far  from  complete  and  the  description 
of  the  sporophyte  given  by  Brebner  (Brebner  3)  fori),  simplicifolia  does  not  deal 
with  the  adult  sporophyte.  The  account  given  here  is  based  mainly  upon  a  study 
of  D.  jamaicensts  and  D.  elhptica,  but  an  investigation  of  certain  points  was  also 
made  in  D.  jenmani.  The  rhizome  in  D.  jamaicensts  and  D.  jenmani  is  a  markedly 
dorsiventral  one.  These  two  species  are  a  good  deal  alike,  but  are  readily  dis- 
tinguished by  the  difterence  in  the  form  of  the  leaves.  In  the  former  the  leaves  are 
rather  larger  and  have  more  numerous  pinnae,  while  the  terminal  pinna  is  developed. 
D.  jctimant  has  somewhat  smaller  leaves  with  from  seven  to  nine  pairs  of  leaflets, 
and  the  leaves  are  abrujitly  ])innate,  tlie  terminal  pinna  not  being  developed  ( plate  q. 


A.  fig^  ,). 
1  he 


leaves  are  arranged  very  much  as  they  are  in  llchntiittiostdilivs  01  in 
Ophtoglossum  penJtilnm,  the  fleshy  leaf  base  being  provided  with  two  vei\  conspic- 
uous stipules  which  are  developed  very  early  in  the  life  of  the  sporoph\  tc.  I'lic 
exact  number  of  roots  corresponding  to  a  leaf  is  not  easv  to  make  out,  but  there  are 
at  least  two,  and  it  is  (juite  possible  that  the  number  may  sometimes  be  greater. 
These  roots  branch  freely,  especially  toward  the  tips. 

D.  clliptica  (plate  lo)  is  a  good  deal  larger  than  the  other  species  and  the  stout 
rhizome,  which,  including  the  persistent  leaf  bases,  has  a  diameter  of  3  centimeters 


176 


THE    MARATTIALES 


or  more,  is  upright,  the  leaves  being  spirally  arranged  as  they  are  in  Marattia  and 
Angiopteris.  The  petioles  in  this  species  are  characterized  by  curious  enlargements 
or  nodes,  which  may  occur  in  the  other  species  also,  but  are  much  less  prominent. 
The  leaves  of  D.  elliptica  reach  a  length  of  about  50  centimeters  and  the  leaflets, 
which  are  much  larger  than  those  in  the  other  species,  are  less  numerous,  there  being 
usually  about  eleven.  The  conspicuous  nodose  swellings  seen  in  the  petiole  are 
repeated  on  a  smaller  scale  in  the  rachis  at  the  base  of  each  pair  of  leaflets.  Sections 
of  the  stems  were  examined  in  D.  jamaiceiuis  and  D.  flliptica,  which,  e.xcept  for  a 
difference  in  size,  agree  closely  in  their  structure.  The  ground  tissue,  as  was  first 
pointed  out  by  Kiahn,  consists  entirely  of  parenchyma,  through  which  are  scattered 
many  conspicuous  tannin  sacs  which,  in  preserved  material,  appear  to  the  naked  eye 
as  numerous  black  specks.  The  section  of  the  vascular  cylinder  looks  very  much 
like  that  of  the  younger  sporophytes  already  described,  but  the  number  of  bundles 
seen  in  the  section  is  larger,  and  there  is  a  group  of  .several  bundles  instead  of  the 
single  medullary  strand  seen  in  the  section  of  the  younger  stem.  In  a  section  from 
a.  large  specimen  of  D.  elliptica  in  which  the  rhizome,  including  the  old  leaf  bases. 


was  about  3  centimeters  in  diameter,  the  outer  ring  ot  bundles  containid  thirteen, 
while  within  this  was  a  smaller  circle  composed  ot  five  medullary  bundles,  three 
large  ones  and  two  smaller  ones.  In  a  similar  section  of  a  medium-sized  section  of 
D.  jamaicensis,  in  "which  the  rhizome  was  about  half  the  size  of  that  in  D.  elliptica, 
there  were  nine  bundles  in  the  outer  ring  and  four  in  the  middle,  two  large  ones  and 
two  small  ones.  In  this  section  the  junction  of  a  root  was  cut  through  and  the  root 
stele  was  seen  to  be  applied  by  its  broad  base  to  one  of  the  larger  of  the  medullary 
bundles  (fig.  161,  J). 

The  relation  of  this  central  group  of  bundles  in  the  stem  to  the  prinuu)- medullary 
strand  was  not  investigated.  Brebner  has  shown  that  in  the  later  stages  of  the  3'oung 
sporophyte  in  D.  simplicifolia  the  original  medullary  strand — which,  as  we  have  seen, 
is  really  the  only  part  of  the  vascular  system  which  is  strictly  of  cauline  origin — 
fuses  at  certain  points  with  the  bundles  of  the  outer  ring,  and  at  this  point  of  fusion 
there  may  be  a  liranching  so  that  a  section  above  this  shows  two  of  these  medullary 
bundles.    Whether  all  of  the  central  group  of  bundles  seen  in  the  stem  of  the  adult 


/;. 


177 


(1  D.  rlliptuii  aif  line  to  iuitlui    l)i aiuliinj;  of  tlic 

uiline 


primary  incdiillary  strand,  or  whether  some  of  thtin  may  be  new  bundles 
oiigin,  remains  to  be  investigated. 

The  arrangement  of  the  characteristic  mucilage  ducts  is  the  same  in  the  two  species 
studied.  There  is  a  ring  of  these  in  the  outer  region  of  the  cortex  and  a  second  group 
in  the  central  region,  these  central  ones  usually  being  close  to  the  vascular  bundles. 


lizoinc  of  Dtifuea  jamtiUcui 
:oi  D.  el  1 1 /yi  lea.     X  i  .5. 
lagc  ducts  arc  not  shown. 


THE  AN.ATOMY  OF  THE  LE.'Vl-. 

A  section  of  the  petiole  of  the  adult  leaf  appears  very  much  like  a  similar  section 
of  the  stem,  except  that  there  is  developed  in  the  cortical  region,  separated  by  several 
rows  of  cells  from  the  epidermis,  a  band  of  sclerenchyma,  yellowish  or  brownish 
in  color,  and  very  much  indeed  like  that  common  in  the  typical  ferns.  Holle's 
statement  that  a  similar  mantle  of  sclerenchyma  occurs  in  the  stem  was  shown  to 
be  an  error,  the  result  of  his  having  investi- 
gated a  fern  which  was  not  a  Daticea. 
There  certainly  was  no  trace  of  scleren- 
chyma in  any  of  the  specimens  I  have 
examined. 

The  distribution  of  the  vascular  bun- 
dles in  the  petiole  is  very  similar  to  that  in 
Hclnunthostachxs,  except  that  inside  the 
ring  ot  bundles  there  is  a  single  larger 
central  one,  instead  of  the  two  small  ones 
which  occur  in  Helminthostachys.  All  the 
bundles  are  continued  into  the  stem  as 
separate  strands  or  there  may  be  a  certain 
amount  ot  anastomosing  among  them,  as 
there  is  in  Ophioglosstim  pendulum,  which 
Daneea  resembles  more  in  the  character  of  its  leaf  traces  than  it  does  Helmin- 
thostachys, where  the  bundles  of  the  petiole  are  united  into  a  single  trace  within 
the  cortex  of  the  stem. 

The  distribution  of  the  mucilage  ducts  in  the  petiole  is  very  much  like  that  of 
the  stem.  There  is  a  definite  ring  of  these  inside  the  zone  of  sclerenchyma  and  several 
larger  ones  in  the  central  region,  near  the  vascular  bundles.  1  he  form  and  venation 
ot  the  leaf  is  essentially  the  same  as  in  the  younger  sporoph\tes  which  have  alread\' 
been  described,  and  stomata  are  developed  only  upon  tiie  lower  side,  the  epidermal 
cells  showing  a  strongly  undulate  outline,  except  tor  the  series  ot  narrow  cells  which 
12 


178 


THE    MARATTIALES 


immediately  surround  the  stoma.  A  section  of  the  lamina  presents  an  appearance 
very  much  like  that  of  Hclninithnstachys.  Below  the  upper  epidermis  is  a  well- 
developed  palisade  layer,  while  below  this  the  spongy  mesophyll  has  the  characteristic 
intercellular  spaces  found  in  the  leaves  of  most  of  the  higher  plants.  Dancea  tricho- 
manoides,  a  very  small  species  from  Peru,  has  delicate  membranaceous  leaves,  which 
probably  would  show  a  much  simpler  structure  than  that  of  the  coriaceous  leaves 
of  the  larger  species.  D.  siiitciisis,  a  species  from  Porto  Rico,  which  is  in  the  herba- 
rium of  the  British  Museum,  has  adventitious  buds  developed  at  the  leaf  tip. 


A,  B.  Two  lont^itudinal 

and  third  leav 

C.  Stem  apex.     XiSi 


Tig.  163. 
:tions  of  a  young  sporophyte  of  Kaulju 
;  r',  second  root.     X20. 
D.  Apex  of  third  leaf.     XiSo. 


THE  APICAL  GROWTH  OF  THE  ROOTS. 

The  earlier  roots  grow  from  a  single  initial  cell,  but  this  is  later  replaced  by  a 
group  of  similar  initials  which,  in  the  large  roots,  are  very  much  like  those  described 
for  the  root  apex  of  Jngioptcris  (Koch  1).  Figure  162  shows  a  section  of  a  root 
from  the  young  sporophvte  which  is  somewhat  transitional  in  character  between  the 
form  with  a  single  detinue  mitial  cell  and  the  larger  root  with  its  group  of  initials. 
The  cell  x,  which  is  very  much  like  the  apical  cell  of  the  primary  root,  may  perhaps 
still  be  considered  as  the  single  apical  cell,  but  the  adjacent  segments  are  almost 
equal  in  size  to  this,  and  it  is  clear  that  they  contribute  to  the  plerome  cylinder  of 
the  root  as  well  as  to  the  cortex  and  the  root  cap. 

In  sections  of  large  roots  taken  from  the  adult  sporophyte,  there  is  found  at  the 
growing  point  not  a  single  initial  cell,  but  a  group  of  apparently  similar  initial  cells 
somewhat  wedge-shaped  in  longitudinal  section  and  arranged  in  a  radiating  fashion. 
No  single  one  of  these  can  be  clearly  recognized  as  a  primary  initial  cell.  These 
cells  divide  at  intervals  by  longitudinal  walls  and  from  the  bases  additions  are  made 


Till-     OLDI-K    Sl'OKOl'IIVTE  179 

to  the  plerome  cylinder,  while  from  the  outer  cells  of  the  meristem  group  arise  the 
new  cells  for  the  root  cap.  The  outer  segments  cut  oft'  from  the  peripheral  cells  of 
the  apical  group  of  cells  undergo  more  rapid  periclinal  divisions  than  those  nearer 
the  center  and  the  cells  thus  formed  contribute  to  the  cortex  of  the  root. 

Unlike  the  roots  of  most  of  the  Ophioglossaces,  those  of  Daitam  branch 
freely  in  a  monopodial  fashion.  This  is  paralleled  among  the  Ophioglossacex-  by 
some  of  the  larger  species  ot  Botryc/iiuni,  Helninithostachys,  and  (Jphioglossum 
pcnJuhini.  Kiihn's  statement  that  the  roots  are  unbranched  is  incorrect.  The 
branching  of  the  roots  was  perhaps  somewhat  more  frequent  in  D.  jamaicensis 
than  in  D.  elliptica,  but  the  latter  species  also  shows  numerous  short  lateral  rootlets. 
The  root  hairs  are  not  conspicuous  on  these  older  rf)ots,  but  are  readily  seen  upon 
the  younger  ones  and  are  then  found  to  be  multicellular,  as  was  first  shown  by 
Brebner  for  D.  simplicifolia.  Sections  ot  the  larger  roots  were  examined  in  these 
two  species  and,  while  they  agreed  in  the  main,  there  were  some  slight  difterences. 
In  a  large  root  of/),  elliptica,  about  2  millimeters  in  diameter,  the  outer  portion  was 
occupied  by  about  four  rows  of  brownish  thin-walled  cells,  very  probably  more  or 
less  suberized.  Within  this  was  a  ring  of  brownish  sclerenchyma  cells  about  three 
cells  in  thickness,  and  between  this  and  the  exceedingly  conspicuous  endodermis  was 
a  broad  zone  of  parenchyma,  the  cells  containing  much  starch.  A  short  distance 
outside  of  the  endodermis  was  a  ring  of  conspicuous  mucilage  ducts.  There  were 
twelve  xylem  rays  alternating  with  as  many  rays  of  phloem.  These  did  not  extend 
to  the  middle  of  the  stele,  which  was  occupied  by  a  pith  of  considerable  size. 
The  roots  of  Z).  jamaicensis  were  somewhat  smaller  and  the  main  diff"erences  were: 
first,  the  thicker  layer  of  tissue  outside  the  ring  of  sclerenchyma,  which  was  much 
less  developed  than  in  D.  elliptica  (in  many  places  this  ring  was  but  one  cell  in 
thickness  and  very  seldom  more  than  two  cells);  second,  the  mucilage  ducts  were 
relatively  very  much  larger;  third,  there  were  but  nine  xylem  masses  instead  of  the 
twelve  in  the  root  of  D.  elliptica. 

The  endophyte,  which  is  usually  found  in  the  primary  roots  of  all  the  Marat- 
tiaceie  is  generally  wanting  from  the  larger  roots  of  the  adult  sporophyte. 

THE  SPOROPHYTE  OF  KAULFUSSIA. 

The  deveK)pment  of  the  young  sporophyte  in  Kaulfussia  resembles  that  of 
Dancea  in  most  respects,  but  from  the  first  it  is  markedly  dorsiventral,  like  the 
sporophyte  of  Helninithostachys.  The  cotyledon,  while  not  provided  with  the  char- 
acteristic free  stipules  of  the  later  leaves,  still  has  its  base  connected  with  a  ridge 
which  extends  around  the  stem  apex  and  youngest  leaves,  which  thus  lie  in  a  cavity 
at  the  base  of  the  cotyledon  in  much  the  same  way  that  the  stem  apex  is  situated  in  the 
young  sporophyte  of  Ophioglossum;  but  the  sheath  in  Kaulfussia  forms  a  shallow 
open  cup,  instead  of  the  closed  conical  sheath  found  in  Ophioglossum.  This  stipular 
sheath  seems  to  be  in  all  respects  similar  in  its  origin  to  that  found  in  Ophioglossum. 

The  second  leaf  lies  nearly  opposite  the  first  and  thi-  thirtl  next  to  the  fiist, 
and  so  on,  the  distichous  arrangement  being  evident  from  the  beginning.  \\'e  have 
already  pointed  out  that  in  the  very  young  sporophyte  the  vascular  bundle  from  the 
cotyledon  is  continued  directly  into  that  of  the  root  and  that  the  bundle  from  the 
second  leaf  joins  this  common  bundle,  as  shown  in  fig.  163.  These  primary  bundles 
run  on  one  side  of  the  apical  meristem,  which,  as  in  Damra,  is  of  very  limited  extent 
and  does  not  contribute  at  all  to  these  bundles. 

The  apical  cell  of  the  young  sporophyte,  up  to  the  oldest  stages  that  were  in- 
vestigated, is  very  much  like  that  of  the  very  young  plant  and  is  broader  than  that 
of  Daiicca,  more  resembling  both  in  cross  and  longitudinal  sections  the  apical  cell 


180 


THE    MARATTIALES 


oi  Ophioglossum.  The  young  leaves  arise  right  and  left  in  succession  on  either  side 
of  the  stem  apex,  and  from  a  very  early  period  are  strongly  bent  over,  showing  the 
characteristic  circinate  vernation  of  the  Marattiaceie.  Sections  made  through  the 
apex  of  the  young  leaf  show  that  it  has  at  first  a  definite  apical  cell  a  good  deal  like 
that  which  is  found  in  the  stem  apex,  and  although  no  satisfactory  cross-sections  of 
this  apical  cell  were  found,  there  seems  to  be  no  question  that  there  is  present  a 
single  definite  initial  cell  which  probably  has  much  the  same  form  as  that  of  the  stem 
apex.  The  young  leaf,  at  this  stage,  has  the  dorsal  region  strongly  convex  and 
composed  of  large  parenchyma  cells.    The  apex  is  bent  over  forward  and  downward. 


Fig.  164.— Scries  ol 
leaf 
D.  Stem  apex  more  enlarged. 
F-H.  Central  region  of  the 

The  tissues  of  the  apex  and  the  adjacent  region  are  composed  of  small,  actively 
dividing  cells.  The  young  vascular  bundle  can  be  clearly  seen  extending  nearly  to 
the  apex  and  continuing  downward  into  the  stem  until  it  joins  the  bundle  from  the 
next  older  leaf. 

The  second  root  arises  at  about  the  same  time  that  the  third  leaf  is  recognizable 
and  apparently  its  origin  is  exactly  the  same  as  it  is  in  Daiura.  Its  stele  joins  the 
central  bundle  of  the  stem  near  its  junction  with  the  third  leaf  trace.  The  young 
leaves,  like  those  in  Daiia-a,  are  sparingly  covered  with  hairs  and  scales,  but  these 
scales  do  not  have  the  peltate  form  found  in  Datura,  being  usually  short  rows  of 
stout  cells;  or  the  hair  may  have  its  base  composed  of  an  oblong  mass  of  cells 
attached  by  a  narrow  stalk  and  having  its  apex  drawn  out  into  a  slender  filament 
composed  of  two  or  three  elongated  cells.  The  terminal  cells  of  these  hairs  usually 
stain  very  strongly,  indicating  that  they  contain  tannin. 

The  young  leaves  are  relatively  stouter  than  in  Dnnera,  but  otherwise  resemble 
them  closely.  In  the  young  sporophyte,  up  to  the  time  of  the  formation  of  the  third 
leaf,  there  may  be  no  trace  of  the  mucilage  ducts,  although  these  may  be  developed 


Till-:    OLDKR    SPOROl'IiyTI-  181 

at  an  earlier  ixriod.  I'lie  mucilage  ducts  throughout  the  hte  of  the  sporophyte 
are  less  conspicuous  in  K/iiiI/iismh  than  in  Daiuca. 

A  section  taken  at  the  level  of  the  stem  apex  in  the  viiy  \nung  s|)<)rophyte 
(fig.  137)  presents  an  appearance  not  unlike  that  found  in  the  bud  in  Oplnuglossutri. 
The  base  of  the  cotyledon  extends  around  the  stem  apex,  so  that  in  the  section  the 
stem  apex  and  the  second  leaf  are  inciosetl  in  this  cavity  formed  by  the  stipular 
sheath  of  the  cotyledon.  Higher  up,  the  base  of  the  cotyledon  becomes  free  from  the 
second  leaf,  but  this  takes  place  earlier  on  one  side  than  on  the  other. 

The  development  of  the  vascular  system  in  the  stem  is  exactly  as  it  is  in  Daiicca. 
The  stem  apex  in  the  young  sporophyte  takes  no  part  in  the  development  of  the 
vascular  bundles,  the  stele  in  the  stem  being  made  up  entirely  of  the  united  leaf 
traces.  In  the  specimen  figured  (fig.  164),  in  which  the  second  leaf  was  still  quite 
young,  the  bundle  from  the  cotyledon  passes  downward  into  the  stem  and  continues 
its  downward  course  until  it  joins  the  second  leaf  trace.  The  resulting  solid  stele 
at  first  shows  the  two  separated  xylems  of  the  component  leaf  traces  which  lower 
down  merge  into  a  single  thick  band  of  xylem  completely  surrounded  by  the  phloem 


(fig.  164,  E-H).  This  stage  corresponds  to  Brebner's  "haplostele"  in  DancFa  sini- 
pUcifoUa.  This  condition  merges  insensibly  into  the  primary  root  with  its  diarch 
bundle,  the  two  xylems  in  the  younger  part  of  the  root  being  quite  separate,  but 
forming  a  single  band  at  the  base  of  the  transitional  region,  between  the  root  and 
the  bundle  in  the  stem.  The  bundle  of  the  root  shows  a  conspicuous  endodermis 
which  becomes  less  and  less  evident  in  the  transitional  region,  although  it  prob- 
ably never  quite  disappears.  The  primary  root  usually  shows  the  presence  of  an 
endophytic  fungus  like  that  occurring  in  the  prothalh'um  and  in  the  priniarv  root 
of  most  of  the  Ophioglossaceae. 

Fig.  166  shows  cross-sections  of  a  young  sporophyte  in  which  the  fifth  leaf  is  still 
quite  small,  but  with  its  trace  showing  the  first  tracheary  tissue.  This  fifth  leaf  trace 
unites  below  with  the  trace  from  the  fourth  leaf  and  forms  a  single  bundle,  with 
the  xylems  separate.  The  xylem  from  the  fourth  leaf  above  its  junction  with  the  fifth 
leaf  trace  forms  at  first  a  continuous  band  which  divides  into  two  parts,  one  of  which 
unites  with  the  xylem  from  the  fifth  leaf  trace,  while  the  other  remains  distinct. 
This  separation  of  the  xylem  in  the  fourth  leaf  trace  is  the  first  indication  of  the  for- 
mation of  the  double  leaf  trace,  such  as  we  shall  find  occurs  in  the  later  leaves. 


182 


THE    MARATTIALES 


The  separated  xylems  become  joined  lower  down  into  a  single  transverse  plate,  just 
before  the  junction  of  the  strand  with  the  trace  from  the  third  leaf  (fig.  i66,  H), 
with  which  it  joins  in  the  same  way  and  is  continued  downward  to  the  junction  with 
the  strand  arising  from  the  fusion  of  the  second  leaf  trace  with  the  cotyledon.  Above 
the  junction  of  the  first  and  second  leaves,  the  stele  of  the  second  root,  which  grows 
vertically  downward,  joins  the  stele  formed  by  the  junction  of  the  three  youngest 
leaf  traces. 

Above  the  junction  the  section  of  the  bundle  is  nearly  circular  in  outline,  the 
large  tracheids  forming  a  broken  group  in  the  center  of  the  bundle,  quite  like  a 


A-C.  Serif 

D.  Stem  apex. 
H-J.  Three  sections  lower  down. 

K.  Central  vascular  cylinder  still  lower  down. 

corresponding  stage  in  Dancrn.  Some  of  the  cells  adjacent  to  the  bundle  show  the 
typical  thickenings  on  the  radial  walls,  indicating  that  they  belong  to  the  endodermis, 
but  the  limits  of  the  endodermis  are  e.xtremely  vague.  In  this  plant  two  mucilage 
ducts  had  developed  in  the  fourth  leaf,  one  on  each  side  of  the  vascular  bundle 
(fig.  1 66,  B,  m). 

The  second  root  is  stouter  than  the  primary  one  and  its  bundle  is  triarch.  The 
mycorrhiza  present  in  the  first  root  could  not  be  detected  in  the  second  root,  but 
possibly  may  be  developed  at  a  later  stage.    All  of  the  roots  are  provided  with  root 


THT    OLDPR    SrOROPFn'Tr 


183 


hairs,  wliicli  rcseniblf  tliost-  in  Diuin-n  in  bLiiii^  iiuiltinlliilai.  In  rlic  laif^er  roots 
there  may  sometimes  he  five  or  six  cells,  each  with  a  conspicuous  nucleus,  makinj; 
up  these  root  hairs,  and  sometimes  they  show  signs  of  branching  at  the  apex. 

It  is  evident  that  in  Kaulfiissui,  up  to  the  time  that  five  leaves  have  developed, 
the  vascular  system  ot  the  stem  consists  of  a  single  axial  strand,  a  sort  of  sympodium 
formed  by  the  completely  united  traces  of"  the  young  leaves.  The  xylem  may  appear 
as  a  sin-gle  mass  at  the  points  where  fusion  of  the  leaf  traces  is  complete,  but  at  most 
points  the  individuality  of  the  component  strands  is  maintained,  so  far  as  the  xylem 
is  concerned. 

Figure  i68  shows  transverse  sections  from  a  iiuuh  older  sporophyte.  The 
section  of  the  petiole  still  shows  the  single  vascular  bundle  having  near  its  inner  face 
a  single  large  mucilage  duct,  which  follows  the  leaf  trace  downward  into  the  stem. 
As  the  bundle  from  the  leaf  enters  the  stem  it  broadens,  and  there  is  a  separation 
of  the  xylems  into  two  masses,  first  seen  in  the  fourth  leaf.  In  the  specimen  shown 
here  the  earliest  leaves  w-ere  not  sectioned,  and,  as  it  can  not  be  stated  exactly  how 
many  leaves  the  young  sporophyte  had  developed,  it  must  therefore  remain  uncer- 
tain which  leaf  first  shows  the  completely  divided  leaf  trace.  In  the  specimen  in 
question  the  oldest  leaf  that  showed  had  a  single  trace  with  two  separate  xylems, 


while  the  next  leaf  had  the  leaf  trace  completely  separated  and  resembling  a  corre- 
sponding stage  in  Datia-a  (fig.  i68,  /').  As  the  traces  from  the  two  leaves  approach 
preliminary  to  their  fusion,  the  double  leaf  trace  has  its  parts  united  again  so  that 
the  traces  become  single  before  they  join.  The  leaf  trace  now  forms  a  single  bundle, 
crescentic  in  section  and  very  much  like  the  single  broad  leaf  trace  from  the  earlier 
leaf.  The  two  traces  come  nearer  and  nearer  and  finally  fuse  on  one  side,  so  that 
a  section  shows  a  single  bundle  almost  circular  in  form,  but  broken  on  one  side 
(fig.  1 68,  H).  This  break  is  finally  closed  up,  and  the  section  of  the  bundle  is 
completely  circular  and  resembles  very  closely  that  oi  Botrxchiutn  or  HfUniutlios- 
taclixs,  except  that  phloem  is  developed  inside  the  ring  of  xylem  (fig.  168,  A").  A 
similar  condition  may  sometimes  be  f^ound  for  a  very  short  rime  in  the  voung  plant 
of /3rt,/,jv/ also. 

No  certain  evidence  of  an  internal  endodermis  coidd  be  made  out  ami  tlu' 
external  endodermis  is  also  somewhat  vague,  although  there  is  pn>babl\-  no  question 
of  its  presence.  The  outer  phloem  is  bounded  by  a  fairly  well-defined  peric\cle, 
between  which  and  the  starch-filled  cortical  cells  of  the  stem  arc  two  or  three  layeis 
of  transparent  cells,  some  of  which  presumably  constitute  the  endodermis.  The 
endodermis  is  certainly  present  in  the  free  leaf  traces,  although  less  conspicuous 


184 


THE    MARATTIALES 


than  it  is  in  the  roots.  In  the  upper  region  of  the  stem  the  leaf  traces  are  further 
apart,  and  as  the  number  increases  a  cross-section  of  the  stem  shows  a  circle 
of  separate  bundles  closely  resembling  the  arrangement  in  Ophioglossum.  The 
central  "commissural"  strand,  which  is  found  in  the  adult  stem,  had  not  developed 
in  any  of  the  young  sporophytes  I  examined  and  evidently  arises  much  later  in  the 
history  of  the  sporophyte  than  it  does  in  the  other  Marattiaceae.  In  this  respect, 
as  well  as  in  the  arrangement  of  the  bundles  themselves,  Kaulfiissia  is  more  like 


A,  B.  Two  sections  above  level  of  stem  a 

C-J.   Sections  taken  lower  down  from 

K.  Central  bundle  of  section  J.      XI, 

L.  Part  of  the  bundle  of  section  H, 


of  a  young  sporophyte  of  Kaulju 
series,    m,  mucilage  ducts. 


enlarged.     G,  F,  I,  J,  show  only  the 


I  of  about  same  age  ; 


Ophioglossum  than  it  is  like  the  other  Marattiaceae.  In  the  intermediate  condition 
between  the  single  solid  stele  found  in  the  very  young  stem  and  the  entirely  separated 
leaf  traces  of  the  older  rhizome,  there  is  a  transitional  condition  with  a  "siphono- 
stele,"  very  much  as  in  Helminthostachys  (fig.  i68,  K). 

In  one  very  young  sporophyte  there  was  found,  in  the  cortex  of  the  primary 
root  near  its  base,  a  large  lacuna  which  recalled  the  similar  lacuna  found  in  the 
first  internode  o{  Helminthostachys. 


HK    OLDER    SPOROPHYTE 


185 


Tlu-  youiig  s[)on)\^h\tv  (>{' Kaiilfussid  is  almost  completely  destitute  of  the  tannin 
cells  which  are  so  conspicuous  a  feature  in  Datura,  and  these  tannin  cells  are  prac- 
tically entirely  absent  from  the  sporophyte  throughout  its  whole  existence.  In  this 
respect  there  is  a  marked  resemblance  to  Opliioglossuni.  The  mucilage  ducts  are 
also  somewhat  less  developed  than  in  the  other  Marattiace:e  and  are  mainly  con- 
lined  to  the  central  part  of  the  stem  in  proximity  to  the  vascular  bundles.  At  a  late 
period  they  may  also  appear  in  the  cortical  region.  Their  lysigenous  origin  is  less 
evident  than  in  Dancea  and  it  is  not  impossible  that  they  may  sometimes  be  of 
schizogenous  origin,  as  Brebner  states  is  often  the  case  in  Dancea. 

The  structure  of  the  vascular  strands  is  very  much  like  that  of  Dancva,  as  a 
reference  to  the  figures  will  show.  There  are  developed  slender,  spirally-marked 
protoxylem  elements  like  those  in  Dana-a  and  which  we  have  already  seen  occur 
also  among  the  Ophioglossace^,  in  Helminthostachys. 

The  stipules  in  the  young  plants  of  Kaulfiissta  are  much  less  definite  than  they 
are  in  Daiicca.  A  cross-section  through  the  bases  of  the  young  leaves  shows  that 
instead  of  the  bases  appearing  free,  each  with  its  distinct  stipules,  the  leaf  is  confluent 
with  the  next  one,  one  side  being  slightly  extended  and  free.  The  leaf  base  thus 
incloses  the  next  younger  leaf  completely  on  one  side,  but  leaves  it  free  on  the 


A.  Bundle  from  intermediate  region  of  .i  \ 

B.  Section  of  primary  root.     X150. 

C.  Section  of  bundle  of  second  root,    fn,  endo 

Other  (fig.  168,  5).  In  the  later  leaves  the  stipules  become  more  conspicuous,  but 
they  are  always  connected  by  a  very  conspicuous  commissure  in  front  (fig.  171,  (oni) 
so  that  a  section  of  the  young  leaf  base  shows  a  space  between  the  front  of  the  petiole 
and  the  stipular  sheath.  In  short,  the  structure  is  very  similar  to  the  open  stipular 
sheath  of  Botrychium  virginianum  and  apparently  arises  in  much  the  same  way. 

The  structure  of  the  adult  sporophyte  has  been  carefully  investigated  by  Kiihn, 
who  pointed  out  that  it  is  the  simplest  of  the  Marattiace:e  in  the  structure  of  the 
stem  (fig.  171,  B).  As  in  the  young  sporophyte,  the  stem  shows  in  section  a  single 
circle  of  vascular  bundles,  but  there  is  in  addition  a  single  median  strand  within  the 
circle  of  bundles  belonging  to  the  dictyostele,  and  this  bundle  is  presuniahl\-  of 
cauline  origin,  like  the  corresponding  one  in  Daiiera. 

The  whole  vascular  skeleton  of  the  stem,  when  removed  by  maceration,  was 
found  by  Kiihn  to  be  a  hollow  cylinder  with  large  open  meshes.  These  are  more 
elongated  on  the  ventral  side  and  from  these  ventral  strands  alone,  according  to 
Kuhn,  the  roots  are  developed.  In  this  respect  Kaiilfiissia  offers  a  certain  analog\- 
to  Helmnithostachys  and  perhaps  to  Ophioglossiini  pendulum. 

As  in  the  other  Marattiaceic,  the  ground  tissue  of  the  rhi/ome  is  composed  of 
simple  parenchyma.  The  outer  layers  have  their  walls  brown  in  color  and  show  the 
reaction  of  cork.     Except  for  the  presence  of  the  central  strand,  a  .section  of  the 


186 


THE    MARATTIALES 


rhizome  oi  Knulfiissin  presents  almost  the  exact  appearance  of  a  similar  section   of 
Ophioglossiini. 

In  a  rhizome  having  a  diameter  of  about  a  centimeter  twelve  bundles  showed 
in  a  cross-section  taken  through  the  internode,  one  of  these  being  the  medullary 
strand.  The  section  of  a  petiole  of  a  leaf  taken  from  the  same  plant  is  shown  in 
fig.  171,  C,  and  the  structure  of  the  section  closely  resembles  that  of  the  rhizome. 
There  were  eight  bundles  arranged  in  a  circle,  within  which  were  two  medullary 
strands.  The  cortical  region  was  composed  of  several  rows  of  brownish  cells,  prob- 
ably similar  to  those  in  the  outer  part  of  the  rhizome,  and  within  these,  separated 


bundle   from   a   young   sporophyte   of   Kutil- 
ftissia,  showing  two  xylems.     X150. 


Fig.  171. 

Rhizome  of  a  large  sporophyte  of  Kaulju 
ules;  com,  commissure.     X]f. 

B.  Section  of  rhizome.     X2. 

C.  Section  of  petiole.     X2. 


from  them  by  three  or  four  rows  of  cells,  was  a  conspicuous  band  of  collenchyma, 
a  tissue  characteristic  of  the  leaves  of  most  of  the  Marattiaceae. 

According  to  Kiihn,  the  bundles  of  the  leaves  are  continued  separately  into  the 
cortex  of  the  stem  and  do  not  unite  into  a  single  leaf  trace.  There  are  occasional 
anastomoses  of  the  vascular  bundles  of  the  petiole,  quite  like  those  in  the  stem  itself, 
and  this  becomes  especially  marked  at  the  base  of  the  leaf,  so  that  the  leaf  trace  (if 
such  it  can  be  called)  forms  a  hollow  reticulate  cone,  quite  equaling  in  diameter  the 
vascular  cylinder  of  the  stem  itself,  and  attached  to  this  by  the  open  base,  the  sepa- 
rate strands  forming  a  crescent-shaped  group  when  seen  in  section.  The  arrange- 
ment of  the  bundles  within  the  petiole  itself  and  their  method  of  junction  with  the 
vascular  system  of  the  rhizome  are  very  much  like  tho.se  in  Ophioglossiim  pendiiluju. 

The  vascular  bundles,  both  in  the  petiole  and  rhizome,  are  concentric.  The 
endodermis  is  not  recognizable  and  the  central  xylem  is  completely  inclosed  by  the 
phloem,  sieve  tubes  being  developed  throughout. 


TIIF 

OI.nivK    SI'OROPMVTi:                                                           187 

\\  hik'  iiuicilafi,i-  diKts  aii'  pre 

■sint  in  hdth  leaf  and  sti-m,  they  aie  less  numerous 

and  conspiiuous  than  in  Daiiua. 

There  is  a  ring  of"  them  in  the  outer  cortex  and 

several  larger  ones  in  the  central  : 

region.     Kidin  states  that,  although  these  mucilage 

ducts  sometimes   look   as  if  they 

were  of  schi/.ogenoirs  origin,   in   reality  the)'  are 

always  lysigenous,  i.  e.,  tiiey  are 

lornu-d  h\   tlie  fusion  of  several  mucdage-secreting 

In  the  cotyledon  and  the  earlier  leaves  a  section  of  the  lamina  shows,  hetween 
the  large-celled  epidermis  of  the  upper  and  lower  sides,  a  mesophyll  composed  of 
about  three  layers  of  (juite  inditierent  parenchyma,  exactly  as  it  is  in  Opiitoglossuni. 
In  the  adult  leaves  the  upper  part  of  the  mesophyll  is  compact,  but  there  is  no 
proper  palisade  tissue  developed.  Toward  the  lower  surface  the  mesophyll  becomes 
looser. 

Until  the  plant  has  reached  a  considerable  si/e  the  leaves  remain  undividetl 
and,  except  for  the  much  greater  size,  closely  resemble  the  early  leaves  of  the  )-oung 
sporophyte  (see  plate  1 1,  fig.  i).  'The  simple  leaves  are  succeeded  later  by  trifoliate 
ones,  and  finally  five  leaflets  are  developed.  The  long,  fleshy  petiole  may  reach  a 
diameter  of  a  centimeter  or  more  and  a  length  of  some  50  centimeters  in  large 
specimens.  The  venation  strikingly  resembles  that  of  a  dicotyledonous  leaf,  the 
pinnately  arranged,  secondary  veins  being  connected  by  a  plexus  of  small  veins, 
inclosing  nearly  square  areoles  within  which  a  few  free  terminations  are  occasionally 
found.  The  large  pores  upon  the  lower  side  of  the  leaf,  formed  by  the  greatly 
enlarged  stomata  already  referred  to  in  the  younger  leaves,  are  plainly  visible  to  the 
naked  eye,  and  sections  of  these  look  curiously  like  the  pores  upon  the  thallus  of 
certain  Marchantiaceae  (fig.  128). 

The  stipules  of  the  older  leaves  are  very  conspicuous  and  show  much  the  same 
structure  as  that  noted  for  the  earlier  leaves.  The  young  leaf  is  included  within  the 
stipular  sheath  of  the  next  older  one,  and  near  the  apex  the  unbroken  stipular  sheath 
of  the  youngest  expanded  leaf  shows  very  plainly  that  the  large  stipules  are  joined 
in  front  by  a  broad  commissure,  which  extends  entirely  around  the  apex  of  the  shoot, 
exactly  as  it  does  in  Helminthostachys,  from  which  the  sheath  differs  mainl}^  in  the 
fact  that  it  is  divided  above  into  the  two  stipules  as  it  is  in  Botrychium  virginiatiiim, 
and  there  seems  no  reason  to  doubt  that  we  have  to  do  with  entirely  homologous 
structures  (fig.  171,  A).  The  stipules  of  the  young  leaves  are  covered  with  hairs 
and  scales  similar  to  those  noted  in  the  young  sporophyte. 

The  roots  arise  from  the  ventral  surface  and  flanks  of  the  rhizome,  and  out- 
number the  leaves,  to  which  they  apparently  bear  no  definite  relation. 

The  apical  growth  was  not  studied  in  the  root  of  the  older  sporophyte,  but  it 
is  probable  that  in  the  large  roots  of  the  older  plant  the  single  apical  cell  found  in 
the  early  roots  is  replaced  by  a  group  of  initials  such  as  are  found  in  the  other 
Marattiaceae,  although  it  is  barely  possible  that  the  single  apical  cell  may  be  retained 
here  as  it  is  in  the  Ophioglossaceae.  Unfortunately,  material  was  not  available  for 
a  study  of  this  point.  1  he  roots  in  most  cases  are  quite  unbranched,  as  they  are  in 
huof^luoglossiitn.  1  he  only  cases  where  branches  were  seen,  were  young  sporoph\tes 
in  which  the  end  of  the  root  had  been  destroyed  and  two  branches  had  arisen  on 
each  side  of  the  destroyed  apex.  This  looks  somewhat  like  a  dichotomy  ami  it  is 
barely  possible  that,  as  in  Opiuoglossum,  there  may  be  a  real  dichotomy  of  the  root, 
but  all  of  the  cases  that  were  found  had  much  more  the  appearance  of  the  formation 
of  two  lateral  roots.  The  young  roots  of  the  sporoph\te  are  provided  with  multicel- 
lular root  hairs,  like  those  of  Dniitiii.  but  these  disappear  as  the  root  becomes  oliler. 
The  ci  nti;d  \;iscid:ir  c\liiuKr  of  the  root  is  surrounded  by  a  circle  of  ver)-  large 
nuicilage  ducts.      TIk  riulocU  1  mis  is  clearly  evident  and  the  routs  which  I  examined 


188  THE    MARATTIALES 

irom  a  medium-sized  plant  were  tetraich.  Kiihn  states  that  pentaich  and  hex- 
arch  roots  also  are  formed.  The  reduced  number  of  xylems  in  the  root  of  Kaul- 
fussia,  as  compared  with  the  other  Marattiaceae,  is  another  indication  of  its  probable 
nearer  relationship  to  the  Ophioglossaceae,  the  structure  of  the  root  being  very  similar 
indeed  to  that  of  Hehninthostachys  or  Ophioglossum  pciulidum. 

TliF.  Sl'UROPIlYTE  OF  MARATTIA. 

The  published  observations  upon  the  young  sporophyte  of  Marattia  are  far 
from  complete.  Kiihn  (Kuhn  I)  has  described  the  stem  structure  in  young  plants 
of  M .  fraxniea,  but  it  is  evident  that  these  plants  were  already  too  far  advanced 
to  show  the  early  arrangement  of  the  bundles,  as  the  stems  he  described  had 
reached  a  length  of  nearly  2  centimeters.  Farmer  and  Hill  (Farmer  3)  have  also 
given  some  details  as  to  the  early  stem  structure  in  the  same  species.  These  young 
plants,  especially  those  described  by  Kuhn,  have  the  stem  relatively  longer  than  is 
the  case  either  in  M.  doiiglasii,  which  I  have  studied  somewhat  in  detail,  or  M. 
alata,  or  M .  sambucina,  which  I  have  also  examined.  In  all  of  these  species  the  stem 
of  the  very  young  sporophyte  is  still  quite  short  and  very  soon  assumes  the  compact 
globular  form  with  the  crowded  leaves  that  it  has  in  the  adult  sporophyte.  It  may 
be  said,  however,  that  in  M.  alata  the  buds  which  develop  upon  the  old  leaf  bases 
have  the  young  stem  somewhat  more  elongated,  but  not  nearly  so  much  as  Kiihn's 
figures  would  indicate  to  be  the  case  in  M.  fraxinea."^'' 

In  the  youngest  specimens  examined  by  Kuhn  the  cross-section  of  the  stem 
showed  a  ring  of  bundles  corresponding  to  the  leaf  traces  and  a  central  medullary 
strand,  the  whole  arrangement  being  very  similar  to  that  which  is  found  in  the 
adult  rhizome  of  Kaiilfiissia.  This  stage  is  also  very  similar  to  the  condition  found 
in  the  young  sporophyte  of  Dancea. 

Farmer  and  Hill  describe  the  vascular  skeleton  of  the  very  young  plant  of  M. 
fraxinea  as  a  "siphonostele"  with  much  larger  foliar  gaps  than  those  found  in 
Angiopteris,  and  thus  more  nearly  resembling  Kaidfussia  or  Dancea.  The  leaf 
traces  are  at  first  single,  but  the  later  leaves  have  double  leaf  traces,  such  as  we  have 
described  in  Dancea  and  Kaidfussia. 

The  writer  has  already  published  some  details  in  regard  to  the  young  sporo- 
phyte of  Marattia  douglasii  (Campbell  3,  4),  and  some  additional  facts  are  here 
added  to  those  that  have  already  been  published;  but  as  the  series  of  specimens 
available  for  study  was  not  at  all  complete,  further  investigation  is  desirable  to 
complete  the  history  of  the  development  of  the  vascular  system  in  Marattia.  The 
only  material  available  for  a  study  of  the  young  sporophyte  in  M.  douglasii  was  a 
series  of  slides  made  a  good  many  years  ago  from  material  collected  on  the  island 
of  Kauai  in  the  Hawaiian  Islands.  This  material  was  supplemented  by  a  small 
number  of  very  young  plants  of  Af.  sambucina,  collected  in  Java.  Material  of  older 
sporophytes  of  M.  alata  was  collected  in  Jamaica  in  the  summer  of  1908.  Un- 
fortunately, all  the  preparations  of  M.  douglasii,  except  the  very  youngest  stages, 
were  longitudinal  sections,  so  that  it  was  diflScult  to  follow  out  satisfactorily  the 
course  of  the  vascular  bundles  in  the  later  stages. 

Longitudinal  sections  of  a  young  sporophyte  before  the  cotyledon  was  com- 
pletely expanded  are  shown  in  fig.  133.  The  section  was  cut  nearly  in  the  plane  of 
the  cotyledon  and  the  bent-over  apex  of  the  latter  was  cut  so  as  to  show  plainly  the 
two  lobes  arising  from  the  first  dichotomy  of  its  apex.  The  second  leaf  is  already 
formed  and  differs  in  no  essential  particular  from  the  corresponding  leaf  in  Kaul- 

*  Since  the  above  was  written  a  paper  has  appeared  (Charles  l)  describing  the  vascular  system  of  the  young  sporo- 
phvtr  of  M. alula.     The  stele  of  the  very  young  plant  is  described  as  a  protosteic  which  passes  abruptly  into  a  solenostele. 


nil.  ()LI)i:k  si'droi'iivti;  189 

fussiti  or  Diiihrii.  It  was  not  (|iiit(.'  ctitain  whctlur  a  siiiiilf  apical  clII  was  |Misent 
at  this  stage,  but  a  triangular  cell  which  could  be  seen  at  the  apex  was  probably 
the  apical  cell  of  the  young  leaf.  The  root  apex  of  this  specimen  had  been  injured 
so  that  the  form  of  the  apical  cell  could  not  be  clearly  made  out,  but  it  was  probably 
the  same  as  we  have  already  described  iov  the  young  sporophyte.  I  he  apical  cell  of 
the  stem  meristem  was  broader  in  outline  than  that  of  Daiuva  and  truncate  below . 
The  vascular  system  at  this  stage,  as  we  have  already  indicated  earlier,  consists 
of  the  common  bundle  of  the  root  and  the  cotyledon,  which  is  joined  at  a  point  quite 
close  to  the  stem  apex  by  the  second  leaf  trace.  The  first  tracheaiy  tissue  is  visible 
at  this  point  in  the  form  of  short,  reticulately  marked  tracheids  such  as  we  have 
already  seen  in  the  young  sporophyte  of  Dcuuva.  At  this  stage  no  mucilage  ducts 
or  tannin  cells  had  develojud.     About  the  base  of  the  young  leaves  are  short  iiaiis 


A,  B.  Two  longitudinal  sections  of 
sporophyte  of  Marattm  ilouglo 
second  leaf;   r' ,  second  root.     X 

C.  Part  of  primary  root,  showing 
fected  by  endophytic  fungus. 


Ho.  173. 
a  young  sporophyte  of  Maraitia 
.    5/,  stem  apex;  /,  young  leaves; 

X2S. 


and  scales  like  those  we  have  seen  in  the  other  genera.    They  are  more  like  those  of 
Kaulfussia  than  like  the  peltate  scales  found  in  Dtuuca. 

Sections  of  a  somewhat  older  sporophyte  are  shown  in  figure  172,  tiiis  section 
being  made  at  right  angles  to  the  one  just  described.  The  cotyledon  in  this  specimen 
was  fully  expanded  and  the  primary  root  had  penetrated  into  the  earth.  I'hc 
arrangement  of  the  bundles  was  the  same  as  in  the  younger  sporophyte  described, 
except  that  the  third  leaf  was  now  visible  and  the  second  root  was  already  well 
advanced.  The  section  passed  exactly  through  this  root,  the  stele  of  which  is  seen 
to  join  that  of  the  second  leaf  and  is  practically  continuous  with  it.  The  young 
trace  fVom  the  third  leaf  joins  the  second  leaf  trace  near  its  junction  with  the  second 
root.  The  apical  cell  of  the  latter  was  readily  seen  and  appears  in  longitudinal 
section  of  nearly  triangular  form,  but  with  the  base  somewhat  truncate  (fig.  177,  C). 
The  tracheaiy  tissue  in  the  middle  of  the  sporophyte  is  pretty  well  advanced 
and  the  formation  of  the  tracheaiy  tissue  has  extended  for  some  distance  into  the 
primary  root  and  the  cotyledon.     In  the  former  a  single  elongated  tannin  sac  could 


190 


THE    MARATTIALI' 


be  seen,  like  those  which  are  much  more  developed  in  the  primary  root  o{  Jrigiop- 
teris,  and  it  was  also  seen  that  certain  of  the  cells  in  the  cortex  of  the  primary  roots 
were  invaded  by  the  endophytic  fungus.  In  the  cotyledon  there  was  a  single  large 
mucilage  duct. 

A  series  of  transverse  sections  was  made  of  a  young  sporophyte  of  M.  sam- 
bucina  and  these  agreed  in  all  essential  particulars  with  similar  sections  of  Daticea 
or  Kaidfiissia. 

In  a  young  sporophyte  of  M.  douglasti,  in  which  two  roots  were  developed  in 
addition  to  the  primary  one,  there  could  be  seen  at  the  apex  two  young  leaves,  prob- 
ably the  fourth  and  fifth,  but  as  only  the  median  sections  of  this  series  had  been 
kept  the  exact  number  of  leaves  could  not  be  determined. 

The  central  part  of  the  stem  in  this  plant  (fig.  173)  was  occupied  by  a  single 
thick  bundle,  but  whether  this  was  solid  or  open  on  one  side,  as  Farmer  states  is 


the  case  in  M.  fraxinca,  could  not  be  satisfactorily  determined.  At  this  stage  the 
section  of  the  young  plant  almost  exactly  resembles  a  similar  one  in  Danira,  and 
presumably  the  single  central  strand  is  composed  of  the  confluent  leaf  traces  from 
the  three  first  leaves,  as  it  is  in  Daiiara. 

The  .xylem  of  the  bundle  is  still  composed  exclusively  of  short,  reticulate  tra- 
cheids.  Large  mucilage  ducts  and  numerous  tannin  sacs  are  developed  in  the 
petioles  of  the  older  leaves  and  the  elongated  tannin  sacs,  like  those  in  the  roots  of 
Daria-a  and  Angiopteris,  are  sparingly  developed  in  the  young  roots;  but  both  tannin 
sacs  and  mucilage  ducts  were  absent  from  the  stem  tissues  at  this  period. 

In  a  still  older  plant  (fig.  174)  the  single  central  bundle  of  the  basal  region  is 
replaced  by  the  separated  steles  of  the  single  leaf  traces,  which  are  beginning  to  form 
the  open  dictyostele  characteristic  of  the  adult  sporophyte.  The  exact  nature  of  its 
origin  could  not  be  followed  in  the  material  at  my  disposal,  but  it  is  presumably 


THK    OLDER    SI'OKOI'HVTr:  191 

mucli  the  same  as  that  (.lescrihtil  for  Dmiati,  since  tlie  ap|)earaiue  of  the  Idii^itiidinal 
sections  in  Marattia  is  exactly  like  that  of  coriespondinj;  sta<;es  in  Duiuni.  The 
apex  of  the  stem,  however,  is  much  broader  than  in  Datia-a.  There  is  in  the  middle 
of  the  apical  region  a  cell  which  from  its  size  and  position  may  be  pretty  certainly 
denominated  the  apical  cell  (fig.  174,  C).  There  is  present  a  strand  of  procam- 
bium  which  ends  abruptly  a  short  distance  below  the  stem  apex.  This  strand 
|irobably  represents  the  primary  commissural  strand,  which,  as  in  Datia-t:,  is  in 
all  probability  a  truly  cauline  bundle  and  has  no  direct  connection  with  the  leaf 
traces.  In  the  central  region  of  the  stem  there  are  now  seveial  large  mucilage 
ducts,  but  tannin  cells  are  still  absent.  In  the  roots,  however,  the  tannin  cells  are 
abundantly  developed. 

Farmer  and  Hill's  brief  account  of  the  development  of  Maratttti  fiaxinea  agrees 
with  my  own  observations  so  far  as  they  have  gone,  except  for  the  interpretation 
of  the  vascular  bundles.  The  "protostele"  found  in  the  lower  part  of  the  stem  is 
undoubtedly  the  common  bundle  of  the  primary  root  and  the  cotyledon,  and  the 
open  "siphonostele"  is  really  made  up  of  separate  leaf  traces,  which  anastomose 
at  certain  points  to  form  the  large  meshes  of  the  very  open  dictyostele.  Farmer  and 
Hill  call  attention  to  the  fact  that  the  "foliar  gaps"  are  much  wider  than  in  Aiigi- 
optcn's,  and  in  consequence  the  separate  strands,  seen  in  section,  form  a  circle  of 
apparently  quite  separate  bundles,  evidently  closely  approximating  the  condition 
found  in  Datuea  and  Kaiilfussia.  Farmer  and  Hill  do  not  make  it  quite  clear  that 
the  commissures  which  they  found  developed  later,  connecting  the  strands  of  the 
dictyostele,  were  really  parts  of  the  central  cauline  strand,  but  they  presumably 
assume  that  such  was  the  case,  as  this  is  explicitly  stated  in  the  case  of  Jngiopteris, 
which  they  also  studied.  The  structure  of  the  bundle  in  the  latest  stage  described 
by  Farmer  and  Hill  agrees  pretty  closely  with  the  condition  described  by  Kiihn  in 
the  youngest  specimens  which  he  studied,  where  the  stem  was  about  a  centimeter 
in  diameter. 

The  early  leaf  traces,  as  in  the  other  Marattiace;e,  are  single,  but  later  on  double 
traces  are  formed.  According  to  Farmer  and  Hill,  the  two  bundles  of  the  leaf  trace 
unite  before  joining  the  vascular  cylinder  of  the  stem.  No  material  was  available 
for  a  further  study  of  the  development  of  the  bundle  in  M.  cloiiglnsn,  bur  it  |irobablv 
agrees  with  that  of  M.  fraxinca. 

Several  young  plants  of  M.  alata  were  examined  for  comparison  with  the  young 
germ  plants  of  M .  douglasii.  The  specimens  in  question  (fig.  175)  had  arisen  as 
adventitious  buds  upon  the  old  leaf  bases  which  had  become  separated  from  the 
stem.  This  manner  of  formation  of  the  young  plants  is  very  common  in  this  species 
(see  plate  12,  A).  In  one  of  these  yt)ung  plants,  in  which  the  stem  was  about  4 
centimeters  long  and  1.5  centimeters  in  diameter,  exclusive  of  the  leaf  bases,  the 
oldest  expanded  leaf  had  a  petiole  of  about  8  millimeters  in  diameter.  In  these 
young  plants  there  is  usually  only  one  leaf  expanded,  so  that  they  have  a  very  different 
appearance  from  the  fully  developed  sporophyte  with  its  crowded  circle  of  leaves, 
and  these  monophyllous  plants  reminil  one  very  much  of  sterile  specimens  of  some 
of  the  larger  species  of  Botrychiutn  (plate  12,  B).  A  section  of  the  petiole  of  this 
specimen  showed  ten  vascular  bundles  arranged  in  a  circle,  within  which,  on  the 
ventral  side,  were  two  other  bundles.  The  section  resembled  almost  exactly  that 
of  the  petiole  of  a  fully  developed  lenf  of  Fffhninf/iostarlivs.  At  the  base  of  the  leaf 
are  the  two  very  conspicuous  stipules,  one  of  which  overlaps  the  other.  These 
stipules  are  connected  by  a  commissure  which  joins  the  two  stipules  near  the  base 
and  is  entirely  concealed  within  the  cavity  formed  by  the  overlapping  stipules, 
but  can  be  seen  on  raising  these,  as  a  hood-like  membrane,  overarching  the  next 


192 


THE    MARATTIALES 


younger  leaf.  Fig.  175,  E,  shows  a  young  leaf  from  another  plant,  in  which  one 
side  has  been  cut  away  so  as  to  show  the  relation  of  the  stipules  to  the  leaf  base. 
This  leaf  was  still  coiled  up  and  its  apex  was  quite  concealed  within  the  large 
overlapping  stipules.  Both  as  to  its  position  and  its  relation  to  the  stipules,  the 
commissure  exactly  resembles  the  lip-like  basal  extension  of  the  stipular  sheath  in 
Botrychiitm  and  Hclminthostachys,  and  there  is  no  reason  to  suppose  that  it  is  not 
exactly  homologous  with  this. 

Partially  inclosed  by  the  stipular  sheath  of  the  expanded  leaf  is  the  next  younger 
leaf,  which  is  cut  in  a  plane  nearly  at  right  angles  with  that  of  the  oldest  leaf,  so  that 
the  overlapping  of  the  stipules,  which  entirely  conceal  the  rest  of  the  leaf,  is  very 
plainly  seen  (fig.  175,  B,  P).  Within  the  stipular  sheath  of  this  leaf  is  a  still  younger 
one,  which  is  entirely  concealed  from  view  from  the  outside,  but  shows  plainly  in 
longitudinal  sections,  taken  next  to  the  center  of  the  bud.  The  stem  apex  is  entirely 
concealed  within  the  sheath  of  the  younger  leaf.    The  resemblance  of  this  section  of 


Fig.  175. — Marattia  alata  Smith. 

The  outer  tissue  has  been  { 


A,  B.  Yuunp  plant  ilcvclopcd  as  a  bud  upon  an  old  I 
of  the  thick  central  section  are  shown.      XI. 

C.  Section  of  petiole  of  leaf. 

D.  Three  sections  of  a  rhizome  of  a  small  plant.     X1.33 

E.  Young  leaf.    The  lamina  is  coiled  up  within  the  large  stipules,  st. 

to  show  the  commissure,  com.      Xl.'^3 


of  the  stipules  has  been  i 


the  young  plant  to  a  similar  section  of  the  bud  in  one  ot  the  larger  species  of  Botry- 
chtum  or  of  Helminthostachys  is  sufficiently  striking. 

The  bundles  forming  the  ring  in  the  petiole  anastomose  freely  in  the  leaf  base, 
as  they  do  in  Kaidfiusia  or  Ophioglossum  poidulum,  so  that  the  number  of  strands 
in  the  leaf  trace  is  smaller  than  the  number  of  bundles  within  the  petiole. 

The  vascular  bundles  in  the  stem  form  a  single  very  open  mesh-work,  with 
which  the  leaf  traces  join  and  which  is,  with  little  question,  composed  entirely  of 
these  leaf  traces,  as  it  is  in  the  earlier  stage.  Indeed,  except  for  the  larger  size  of 
these  plants,  there  is  no  essential  difference  between  them  and  the  young  germ 
plants,  described  in  M.  douglasii.  Several  roots  are  usually  developed  before  the 
first  leaf  of  these  young  bud-plants  unfolds.  Probably  one  root  develops  for  each 
leaf,  but  it  is  not  certain  that  this  is  always  the  case.  Owing  to  the  thickness  of  the 
cortical  region  which  has  to  be  traversed  by  the  root  before  it  emerges,  the  roots 
have  already  reached  a  large  size  before  they  appear  upon  the  outside.    This  deep- 


Till-    OLDKR    SPOROPHYTi;  193 

scatfd  origin  of  tlic  roots  of"  tlu-  Marattiacex*  has  often  liti-n  Hgiinil  and  tk-sriilud. 
The  roots  from  the  base  of  this  plant  showed  the  hexarch  stiuctuie,  the  six  xylem 
masses  being  united  in  the  middle  of  the  stele.  About  half-way  between  the  stele 
and  the  epidermis  of  the  root  is  a  circle  of  large  mucilage  ducts,  but  these  were  quite 
absent  from  the  outer  cortex.  No  mycorrhiza  could  be  found,  except  that  in  the 
outermost  layers  of  cells,  which  constitute  a  iiidimentary  periderm, occasional  fungus 
filaments  can  be  detected,  but  these  are  very  different  in  appearance  from  the 
typical  mycorrhi/.a  found  in  the  primary  root  of  the  germ  plant.  No  root  hairs  could 
be  found,  but  occasionalU'  short  stumps  wire  seen  which  looked  as  if  a  root  hair 
had  been  broken  off. 

Fig.  175,  1),  shows  three  consicurivi'  free-hand  sections  of  a  stem  from  a 
plant  of  about  the  same  size  as  the  one  we  have  just  described,  but  evidently  much 
older,  as  there  were  the  remains  of  many  leaves  and  the  whole  caudex,  except  for 
its  smaller  size,  was  very  much  like  that  of  the  adult  plant.  The  broad  vascular 
strands  made  up  of  the  confluent  leaf  traces  formed  an  irregular  circle  which  in 
fig-  '75'  ^'  ■^'  ii  shows  the  free  central  strand  which  lower  down  forms  the  com- 
missure across  the  central  parenchyma.  The  arrangement  of  the  bundles,  therefore, 
in  the  young  plant  of  Marattiaceae  is  the  same  as  in  the  adult  rhizome  of  Kaulfiissia. 
In  these  sections  two  roots  are  shown,  one  of  which  is  cut  through  the  point  of 
junction  with  a  strand  of  the  dictyostele  (fig.  175,  D,  i).  As  in  the  younger  germ 
plants,  tannin  cells  are  quite  absent  from  the  stem,  although  in  the  roots  they  are 
conspicuous.  A  few  large  mucilage  ducts,  however,  occur  in  the  ground  tissue  of 
the  stem. 

Farmer  and  Hill  give  one  figure  of  a  cross-section  of  the  stele  from  the  young 
stem  of  Maratti (I  which  shows  that  it  has  essentially  the  same  structure  as  that  of 
DatKsa.  There  is  a  fairly  well-marked  endodermis,  within  which  lies  a  broad  zone 
of  phloem,  entirely  surrounding  the  central  mass  of  xylem. 

According  to  Kiihn,  there  is  in  the  older  plant  a  second  circle  of  bundles  within 
the  first,  but  no  satisfactory  account  is  given  as  to  the  relation  of  the  bundles  making 
up  this  second  circle  with  those  of  the  outer  dictyostele.  However,  it  is  probably 
composed  also  of  elements  derived  from  the  leaf  traces,  but  it  is  possible  that  some 
of  the  strands  may  be  of  cauline  origin. 

THE  ADULT  SPOROPHYTE  OF  MARATTIA. 

The  genus  Marattin  includes  about  25  extremely  variable  species,  some  of 
which,  e.  g.,  M.  fraxiuea,  closely  resemble  Angioptcris  in  their  general  habit  (see 
Bitter  1,  page  441;  Christensen  1).  They  occur  in  the  moist,  tropical  regions  of 
both  the  Old  and  New  World,  and  one  species,  M.  salicifolia,  extends  as  far  south 
as  the  Cape  Region  of  South  Africa.  M.  douglasii  is  a  conspicuous  fern  of  the 
Hawaiian  Islands.  This  species  I  have  studied  somewhat  in  detail,  as  well  as  the 
West  Indian  M.  alata,  which  is  abundant  in  the  mountain  forests  of  Jamaica.  These 
two  species  closely  resemble  each  other  in  general  habit  and  have  the  leaves  very 
much  more  divided  than  is  the  case  in  M.fraxitiea  and  its  allies  (see  plate  12). 

The  stem  in  the  adult  plant  is  an  almost  globular,  upright  caudex,  a  foot  or 
more  in  diameter  in  large  plants.  The  closely  set,  spirally  arranged  leaves  have 
very  stout  petioles,  5  or  6  centimeters  in  diameter  at  their  base,  which  is  enlarged 
and  provided  with  two  very  large  wing-like  fleshy  stipules,  which,  with  the  base  of 
the  leaf,  remain  attached  and  completely  cover  the  caudex  after  the  petioles  have 
fallen  away.  There  is  at  the  base  of  the  leaf,  as  in  the  other  Maraftiacent%  a  pulvinus- 
likc  enlargement,  where  the  leaf  breaks  oft",  leaving  a  clean  scar  marked  by  the  broken 
ends  of  the  vascular  bundles.  The  leaves  may  reach  a  length  of  2  to  3  meters  rr 
13 


194 


THE    MARATTIALES 


even  more.  The  thick,  fleshy  texture  of  the  leaflets,  much  Hke  that  of  Botrychium 
tcrnatiim  or  B.  silaifolium,  at  once  distinguishes  Marattia  from  any  of  the  large 
leptosporangiate  ferns  with  which  it  may  be  associated.  The  resemblance  to  the 
leaves  of  Botrychium  is  especially  marked  in  the  young  plants  growing  from  the 
stipular  buds.  These  leaves  show  a  marked  triangular  outline,  curiously  similar  to 
that  of  the  larger  species  of  Botrychium  {ste  plate  12,  B).  The  venation  of  the  leaf- 
lets is  also  very  like,  resembling  that  oi Botrychium  more  than  it  does  that  oi Dancea 
or  Angiopteris.  In  the  species  with  large  linear  leaflets,  e.  g.,  M.  fraxinea,  the  form 
of  the  leaf  is  quite  similar  to  that  of  Jngtoptcris  or  Dainra,  but  the  veins  are  not  so 
closely  approximated. 

The  structure  of  the  leaf  was  particularly  studied  in  M.  alata,  which  closely 
resembles  the  Hawaiian  M.  douglasii.  In  well-grown  specimens  the  leaves  measure 
2  or  3  meters  in  length,  with  a  petiole  which  is  5  or  6  centimeters  in  diameter  above 
the  insertion  of  the  stipules  and  is  somewhat  larger  lower  down.  Where  it  joins 
the  stem  there  is  a  marked  constriction  and  the  leaves  often  become  broken  off  at 
this  point,  the  fleshy  leaf  base  remaining  alive  and  often  giving  rise  to  adventitious 
buds  (plate  12,  A,  3).  A  section  of  the  leaf  base  above  the  stipules  shows  the  vascular 


A.  Section  of  ultimate  rachis  of  a  leallet  of  Marattia  alata.    The  shaded  ; 

B.  Collcnchyina  cells,  more  highly  magnified. 

C.  Part  of  vascular  bundle.    The  shaded  cells  are  tannin  sacs. 


ullcnchvina;  m,  mucilage  du 


bundles  to  be  arranged  in  two  large  concentric  circles,  within  which  is  a  smaller 
third  ring  corresponding  to  the  two  inner  bundles  found  in  the  section  of  the  younger 
leaf.  Below  this  point  there  are  numerous  anastomoses  of  the  bundles  before  they 
enter  the  cortex  of  the  stem,  and  the  leaf  trace  consists  of  a  much  smaller  number 
of  bundles,  eight  in  the  specimen  examined,  which  are  arranged  in  a  single  circle, 
open  on  the  adaxial  side.  The  distribution  of  the  bundles  to  the  stipules  was  not 
studied,  but  it  no  doubt  corresponds  to  that  in  other  species,  where  the  veins  form 
an  extensively  branched  system,  connected  with  the  bundles  of  the  petiole. 

The  large  leaves  of  M.  alata,  when  fully  developed,  are  five-pinnate,  the  ultimate 
leaflets  being  about  2  centimeters  long.  From  the  midrib  extend  lateral  veins  which 
usually  fork  once  but  may  remain  undivided  (plate  12,  A,  i ).  The  bundles  of  the 
rachis  in  the  later  divisions  of  the  leaf  diminish  in  number  and  show  the  horseshoe- 
like arrangement  seen  in  the  leaf  trace  after  it  leaves  the  petiole.  In  the  final  divisions 
the  crescent  of  bundles  seen  in  the  larger  rachis  is  always  completely  united  and 
in  section  appears  as  a  single  horseshoe-shaped  bundle  (fig.  176,  A).  In  the  main 
stipe  and  secondary  and  tertiary  rachis  there  is  a  conspicuous  hypodermal  sheath 
of  sclerenchyma.     This  sclerenchyma  passes  into  collenchyma  near  the  base  of  the 


IHK    0LD1;R    Sl'OKO 


195 


stipe  and  Hnally  disappears  entirely  before  the  stem  is  reached.  1  he  scieienchynia 
is  also  replaced  by  collenchyma  in  the  rachis  of  the  terminal  divisions  of  the  leaf. 
Tannin  sacs  are  quite  absent  except  from  the  immediate  vicinity  of  the  bundles, 
where  they  occur  upon  the  inner  concave  side,  either  in  direct  contact  with. the  bundle 
or  actually  within  it.  1  he  leaf  lamina  is  only  about  half  as  thick  as  that  of  the  leath- 
ery Ics^f  of  Ddiuva  clliptica,  but  shows  much  the  same  structure.  1  he  palisade  cells 
are  not  (juite  so  well  developed  and  there  is  a  complete  absence  of  sclerenchyma,  but 
otherwise  the  structure  is  very  similar.  The  cells  of  the  epidermis  are  undulate  in 
outline  and  the  stomata,  like  those  in  Dana-a,  are  surrounded  by  a  series  of  accessoiy 
cells. 

The  hui^e  roots  may  attain  a  diameter  of  6  to  7  millimeters.  In  the  absence 
of  the  hypodermal  sheath  of  sclerenchyma  they  more  nearly  resemble  Kaulfussia 
than  Daiicea,  but  they  are  more  like  Dancca  in  the  greater  number  of  xylem  rays, 
which  number  twelve  in  the  largest  roots  examined.  In  these  later  roots  the  central 
part  of  the  stele  is  occupied  by  the  pith,  the  xylem  rays  not  being  united  as  they 


f  a  small  root  of  Marattiti  dau^lasii 

B.  I'ranivirse  section  of  apex  of  a  similar  root. 

C.  Longitudinal  section  of  the  apex  of  the  second  r 

D.  Apex  of  a  large  root  of  M.  alata.    x  .v,  initial  cells 


are  in  the  roots  from  the  younger  plant,  but  in  some  cases  a  few  scattereti  tiacheids 
appear  in  the  central  region.  There  is  usually  a  ring  of  conspicuous  mucilage 
ducts  in  the  cortex,  but  these  were  sometimes  not  very  well  developed.  Numerous 
tannin  sacs  are  scattered  through  the  cortex  and  also  occur  within  the  stele. 


THE  SPOI^OPIIYTI';  OK  ANCIOffKRIS. 

AtigiofHcris  is  the  largest  and  most  specialized  of  the  Marattiace;c.  As  we  have 
indicated  before,  there  is  much  difference  of  opinion  as  to  the  number  of  species 
which  should  be  recognized  and  many  botanists  consider  that  all  of  the  forms  belong 
to  a  single  extremely  variable  species.  Bitter,  however,  in  his  account  of  the  Marat- 
tiace;e  in  the  "Natiirliche  Pflanzenfamilien,"  thinks  that  from  20  to  30  species 
should  be  recognized,  following  in  this  respect  the  classification  given  by  Presl  and 
l)e  Vries;  while  Christensen  (Christensen  1)  recognizes  62.  1  have  examined  ma- 
terial from  Australia  furnished  by  Mr.  j.  H.  Maiden,  director  of  the  Botanical 
Gardens  in  Sydney,  as'well  as  material  collected  by  myself  in  Ceylon  and  Java. 
Some  of  the  specimens  growing  in  the  Botanical  Garden  at  Buitenzorg  are  the 
largest  that  I  have  seen.  Leaves  6  meters  and  upwards  in  length  were  measured  and 
the  upright  caudex  was  almost  as  big  as  a  barrel.  The  specimens  seen  in  Ceylon 
were  somewhat  smaller. 


196 


THE    MARATTIALES 


Forms  oi  Angiopteris  occur  from  Polynesia  to  Madagascar  and  northward  as 
far  as  the  Himalayas.     The  genus  also  occurs  in  northern  Australia. 

The  anatomy  of  the  adult  plant  has  been  investigated  more  thoroughly  than 
that  of  any  other  member  of  the  Marattiaceae.  The  most  recent  account  of  the 
anatomy  is  that  given  by  Miss  Shove  (Shove  1),  while  Farmer  and  Hill  have  care- 
fully investigated  the  vascular  system  of  the  young  sporophyte.  A  number  of  prep- 
arations were  made  by  the  writer  for  the  purposes  of  comparison  with  the  other 
genera,  but  no  attempt  was  made  to  follow  out  in  detail  the  extremely  complicated 
vascular  skeleton  of  the  adult  sporophyte.  Farmer  and  Hill  (Farmer  3)  have  given 
a  detailed  account  of  the  development  of  the  vascular  system  in  the  young  sporo- 
phyte ot  Jngioptcns,  so  that  it  was  not  thought  necessary  to  make  a  large  number 
of  preparations  of  this  species,  the  material  of  which  was  collected  at  the  same  place 
where  Farmer  obtained  his  plants.  However,  as  these  authors  did  not  trace  the 
development  of  the  young  bundles  from  the  apical  meristem,  it  seemed  worth  while 
to  examine  this  point  for  the  purpose  of  supplementing  their  account  based  upon 
the  study  of  the  fully  developed  vascular  skeleton. 


young  sporophyt 


The  vascular  system  begins,  as  was  recognized  by  Farmer  in  an  earlier  paper 
(Farmer  1),  as  a  single  strand  connecting  the  root  and  cotyledon,  exactly  as  is  the  case 
in  the  other  Marattiaceae.  In  the  further  study  of  the  development  of  the  vascular  skel- 
eton Farmer  and  Hill  employed  the  method  of  constructing  a  model  of  the  vascular 
system,  built  up  of  superimposed  sheets  of  wax,  corresponding  with  the  outline  of 
the  vascular  bundles  seen  in  the  serial  sections.  The  figures  which  they  give, 
drawn  from  such  models,  show  very  clearly  the  relation  of  the  vascular  strands 
which  make  up  the  complicated  skeleton  in  Angiopteris.  The  assumption  is  made 
that  the  single  stele  found  in  the  young  plant  is  really  a  cauline  structure,  the  leaf 
traces  being  subsidiary.  The  early  history  of  the  vascular  system  of  the  young 
sporophyte  is  given  by  them  as  follows: 

"The  vascular  skeleton  in  the  young  plant  oi  Angiopteris  consists  of  an  axile 
rod  of  tissue,  from  which  strands  are  given  off  to  the  roots  and  leaves  respectively. 
The  first  lateral  root  is  given  off  at  a  point  not  quite  opposite  the  formation  of  the 
first  leaf  trace.  It  is  separated  from  it  by  about  130°.  The  regular  relation  be- 
tween the  leaf  and  the  corresponding  root  is,  however,  soon  lost.  The  gaps  produced 
by  the  early  leaf  traces  are  very  small  and  are  immediately  made  good  above.    The 


IHE    OLDKR 


197 


first  deeply  depressed  aperture  or  gap  occurs  at  about  tlie  sixth  or  seventh  leaf. 
The  leaf  traces  still  continue  to  issue  from  the  stele  as  single  strands  till  a  varying 
number  have  been  formed,  but  they  begin  to  bifurcate  while  still  within  the  cortex 
of  the  stem. 

"As  the  stem  increases  the  leaf  traces  become  more  numerous  and  crowded  and 
they  take  away  a  larger  portion  of  the  vascular  tissue  from  the  axile  strand.  The 
result  is  that  the  leaf  gaps  become  less  rapidly  repaired.  Ihe  stele  is  already  hollow 
in  this  region,  that  is,  it  consists  of  a  cylindrical  vascular  mass  with  perforations 
corresponding  to  foliar  gaps  and  inclosing  a  core  of  parenchyma.  Sooner  or  later, 
the  gap  above  one  leaf  fails  to  be  repaired  until  after  the  exit  of  the  trace  of  the  next 
leaf  and  then  the  original  vascular  cylinder  becomes  broken  up  and  assumes  a 
condition,  in  transverse  section,  conforming  with  that  of  polystely  or  dialystely." 

There  is  thus  a  gradual  transition  from  the  solid  stele  found  in  the  earliest  stages 
to  a  hollow  cylinder  or  siphonostele  with  a  core  of  pith,  and  by  the  formation  of  larger 
and  larger  leaf  gaps  there  is  a  transition  to  an  open  dictyostele  like  that  found  in  the 
other  genera.     Finally  there  appears  the  commissural  strand  which  forms  a  thick 


A-D.  Four  transverse 

the  fusion  of  the 

E.  Centr.il  region  of  C. 

F.  Central  region  of  D 


stem  apex.     B,  C,  s 


strnd  traversing  the  pith  and  undoubtedh'  of  cauline  origin.  This  central  strand 
becomes  more  and  more  important  as  the  plant  develops  and  from  its  central 
position  might  be  mistaken  for  the  original  axial  strand  of  the  young  sporophyte. 
The  vascular  system  at  this  stage  is  described  as  follows: 

"The  leaf  traces  become  more  complex  and  anastomoses  take  place  at  irregular 
intervals  with  the  strands  which  can  still  be  recognized  as  the  relics  of  the  original 
siphonostele,  as  well  as  with  one  another.  Irregularities  also  commence  to  become 
apparent  as  to  the  relative  heights  at  which  the  two  members  of  the  leaf  traces  be- 
come freed  from  the  plexus  of  tissue,  and  a  stage  is  thus  reached  at  which  the  vascular 
skeleton  appears  to  consist  of  a  stout  axile  strand,  surrounded  by  upwardly  diverging 
zones  of  steles,  which  ultimately  pass  out  above  to  the  leaves." 

It  is  evident  that  at  this  stage  there  is  a  condition  which  is  \er\'  much  like  that 
figured  by  Kuhn  for  Kaidfussia,  and  it  is  pretty  clear  that  the  whole  of  the  dictvostele, 
exclusive  of  the  axial  or  commissural  strand,  is  made  up  of  the  "upwardl\-  diverging 
zones  of  steles  which  pass  out  above  into  the  leaves,"  i.  e.,  in  other  words,  the 
dictyostele  is  composed  of  a  union  of  multiple  leaf  traces. 


198 


THE    MARATTIALES 


Transverse  sections  of  a  very  young  sporophyte  of  Angiopteris  show  the  same 
relation  of  the  parts  as  in  the  other  genera.  The  junction  of  the^traces  of  the  first, 
second,  and  third  leaves  takes  place  at  a  very  short  distance  below  the  stem  apex, 
which,  as  Farmer  pointed  out,  shows  an  unmistakable  apical  cell  of  somewhat  irregu- 
lar form.  Compared  with  the  other  genera,  the  primary  leaf  trace  in  Angiopteris  has 
the  xylem  better  developed,  and  composed  of  about  half  a  dozen  tracheids,  where 
the  trace  enters  the  stem.  This  primary  leaf  trace  is  concentric,  as  it  is  in  the  later 
leaves,  and  not  collateral,  as  it  is  in  Daucra  (fig.  179). 

Near  the  point  of  the  junction  of  the  three  primary  traces,  there  may  be  seen 
in  the  young  traces  from  the  second  and  third  leaves  the  first  tracheary  tissue, 
consisting  of  one  or  two  tracheids.  As  the  sections  are  examined  lower  down  the 
tracheary  tissue  of  the  second  and  third  leaf  traces  increases  in  amount  until  it 
forms  a  solid  band,  separated  from  the  corresponding  xylem  of  the  primary  leaf 
trace  by  a  band  of  parenchyma.  The  three  leaf  traces  are  now  completely  fused,  but 
the  sections  of  the  two  xylems  are  perfectly  evident,  and  this  band  of  tissue  between 


A-D.  Four  sections  of  an  older  sporophvte  tha 

E.  Stem  apex.     X130. 

F.  Central  bundle  from  transitional  region. 
O.  Bundle  of  primary  root. 


the  two  xylems  (which  really  belongs  to  the  ground  tissue  of  the  stem  and  not  to  the 
stele  itself)  corresponds  to  the  "pith"  figured  by  Farmer  and  Hill  for  the  transi- 
tional region  between  the  root  and  stem  (fig.  i8o,  C).  Sometimes,  in  still  lower 
sections,  the  two  xylems  are  connected,  but  I  have  found  no  cases  where  the  pith 
was  entirely  surrounded  by  the  xylem,  and  the  two  xylems  of  this  axial  strand  merge 
gradually  into  the  two  xylems  of  the  diarch  primary  root  (fig.  179,  G).  The  endo- 
dermis  is  clearly  evident  in  the  intermediate  region  and  is  recognizable  also  at  higher 
levels,  but  is  less  easy  to  distinguish. 

In  a  series  of  sections,  from  a  plant  in  which  the  fifth  leaf  was  just  recognizable, 
a  section  at  the  level  of  the  stem  apex  shows  the  apical  meristem  to  be  composed 
of  several  large  cells,  one  of  which  is  probably  the  single  apical  cell,  but  this  is  not 
easy  to  determine.  The  base  of  the  fifth  leaf  is  close  to  the  apical  group  and  the 
section  of  its  stele  is  indicated  by  a  group  of  small  cells  close  to  the  stem  apex.  The 
stele  of  the  third  leaf  is  clearly  seen,  separated  from  the  fourth  leaf  by  about  one- 
third  the  circumference  of  the  stem.      Below  the  stem  apex  these  two  leaf  traces 


THK    OI.nFR    SPOROPHVTR 


199 


;ippro;uli,  l)iit  an-  still  srpaiatccl  In  a  cdiisicki al)l(.-  mass  of  tissiit-,  l\ins^  directly 
under  the  stem  apex.  Ihe  two  bundles  finally  join  and  between  them  there  seems 
to  be  a  sort  of  connective  tissue  which  may  perhaps  belong  to  the  stem  itself,  so 
that  this  central  stele  of  the  stem  may  possibly  have  a  certain  amount  of  cauline 
tissue  in  addition  to  that  deiived  from  the  leaf  traces;  but  it  is  quite  as  likely  that 
this  connective  tissue  between  the  bundles  is  nothing  more  than  a  lateral  extension  of 
the  leaf  trace  itself,  very  much  as  is  the  case  in  J / rhuiiit/i'>.^t/ir/iv  and   liatt  \chium. 


.  sporophytc  of  Angioptcr 
r",  r',  second  and  third  roots.    X25.     B,  traverses  the  stem  apei. 

When  the  fusion  is  complete,  the  section  of  the  stele  appears  circular  in  outline 
and  the  whole  of  the  tissue  is  apparently  (piite  uniform,  with  the  exception  of  a  single 
tracheid  marking  the  jiosition  of  the  wleni  of  the  oUler  leaf  trace.  Ihere  follows 
almost  immediateh-  tin-  oUKr  K  :if  trace  which  joins  the  solid  stele,  formed  by  the 
fusion  of  the  traces  tiom  tin-  third  and  fouith  leaf,  witiinut  causing  an\'  break.  At 
this  level  the  first  trachear\  tissue  can  be  seen  in  xhv  fourth  leaf  trace  also.  The 
structure  of  the  stem  below  the  junction  of  the  second  and  third  leaf  traces  is  the 
same  as  that  already  described  for  the  younger  sporophyte.     A  very  young  loot  was 


200  THE    MARATTIALES 

formed  just  opposite  where  the  second  leaf  trace  joined  the  stele.  The  apical  cell, 
which  had  apparently  developed  from  an  endodermal  cell,  had  only  undergone  the 
first  division.  This  root  was  probably  not  the  first  lateral  root,  or  if  it  was,  it  had 
formed  very  much  later  than  is  usual.  The  base  of  the  plant  had  been  somewhat 
injured  and  there  was  what  looked  like  the  remains  of  another  root,  which  was 
probably  the  first  lateral  root. 

The  oldest  specimen  of  which  sections  were  made  had  four  fully  developed 
leaves  and  the  rudiments  of  the  fifth  and  sixth.  An  examination  of  the  lower  series 
of  sections  showed  the  remains  of  one  or  two  other  leaves  and  it  was  probable  that 
eight  leaves  all  together  had  been  formed.  At  the  level  of  the  stem  apex  (fig.  i8i,  5) 
six  separate  leaf  traces  could  be  seen  and  the  relation  of  the  younger  ones  to  the  apex 
was  exactly  the  same  as  in  the  younger  sporophyte.  Below  the  apex,  the  central 
stele  of  the  stem  shows  a  broken  ring  of  procambium  inclosing  larger  parenchyma, 
representing  the  pith.  The  procambium  ring  is  made  up  evidently  of  two  portions, 
one  of  which  is  certainly  referable  to  the  sixth  leaf  trace,  while  the  opposite  one 
perhaps  represents  the  beginning  of  the  next  leaf  trace,  although  the  leaf  to  which 
it  belongs  is  not  yet  evident  above  (fig.  i8i,  D).  The  junction  of  the  leaf  traces  so 
close  to  the  stem  apex  makes  this  point  very  difficult  to  decide. 

The  fusion  of  the  fifth  and  fourth  traces  follows  quickly  and  the  resulting  stele 
shows  plainly  the  three  separate  xylems  of  its  component  bundles.  The  older 
portion  of  the  stele  shows  that  it  is  still  solid,  with  no  evident  leaf  gaps  (fig.  i8i, 
EG),  but  with  several  groups  of  tracheids  probably  corresponding  to  as  many  leaf 
traces,  though  less  distinct  than  in  the  younger  plant.  This  is  complicated  by  the 
fusion  of  the  root  traces,  which  disturbs  the  arrangement  of  the  xylems  from  the 
leaf  traces,  but  the  xylem  is  less  compact  than  is  figured  by  Farmer  and  Hill  and 
the  "pith"  much  less  definite;  indeed,  one  can  hardly  speak  of  a  pith  in  this  connec- 
tion. No  trace  could  be  seen  of  the  central  commissural  stiand  which  later  makes 
its  appearance  and  which  presumably  arises  in  the  same  way  that  it  does  in  Datura. 

In  the  early  stages  Angiopteris  appears  to  agree  closely  with  the  other  Marat- 
tiaceaein  the  development  of  its  vascular  system,  but  the  single  central  stele  without 
leaf  gaps  is  retained  much  longer  than  in  the  other  genera  and  it  also  becomes  much 
larger  and  has  a  better-developed  xylem,  and  the  open  dictyostele,  formed  from  the 
anastomosing  of  the  early  single  leaf  traces,  characteristic  oi'  Dana-a  and  Marattia, 
is  not  present.  It  is  not  quite  clear  whether  the  "siphonostele"  with  its  small  leaf 
gaps,  which  is  the  next  stage  in  the  development,  is  made  up  entirely  of  leaf  traces, 
and  it  is  possible  that  the  stelar  tissue,  connecting  the  adjacent  leaf  traces,  may  be 
composed  in  part  of  cauline  tissue.  On  the  other  hand,  it  is  quite  as  likely  that  the 
connection  of  the  leaf  traces  is  brought  about  merely  by  a  broadening  at  the  point 
of  contact,  such  as  occurs  in  Helminthostachys.  Indeed,  at  this  stage,  the  stele  of 
Angiopteris  is  more  like  that  oi  Helminthostachys  than  like  that  of  the  other  Mafat- 
tiacea?. 

THE  ADULT  SPOROPHYTE  OF  ANGIOPTERIS. 

In  habit  Angiopteris  closely  resembles  the  larger  species  of  Marattia.  The 
enormous  leaves  are  arranged  spirally  about  the  thick  upright  caudex,  which  is 
covered  completely  by  the  persistent  bases  of  the  old  leaves.  The  leaves  are  usually 
twice-pinnate;  the  linear  leaflets  have  more  or  less  conspicuously  serrate  margins 
with  a  venation  very  much  like  that  of  Danaa,  the  veins  being  more  closely  set  than 
in  Marattia.  In  addition  to  the  ordinary  subterranean  roots,  large  aerial  roots  are 
not  infrequent,  but  it  is  doubtful  if  there  is  any  essential  difference  between  the  two 
kinds  of  roots. 


THF    OLDER    SPOROPHYTK  201 

The  anatomy  of  the  stem  closely  resembles  that  of  Marattia,  Inir  the  hiiiulks 
seen  in  section  are  much  more  numerous  and  instead  of  being  arranged  in  two 
circles,  exclusive  of  the  central  commissural  strand,  are  usually  arranged  in  four  or 
five.  The  first  complete  study  of  the  arrangement  of  the  bundles  in  the  stem  was 
made  by  Mettenius  (Mettenius  2).  A  summary  of  his  results  is  given  in  the  paper 
by  Miss  Shove.  Briefly  stated,  Mettenius  describes  the  distribution  of  the  bundles 
as  follows  (Shove  I,  p.  498): 

"The  vascular  bundles  form  funnel-shaped  zones,  with  their  lower  ends  in  the 
axis  of  the  stem  and  their  upper  portions  continued  out  into  the  leaves  as  leaf  traces. 
It  is  the  transverse  sections  of  these  concentrically  arranged  funnels  which  appear 
as  the  rings  of  separate  bundles  in  the  section  of  the  stem.  Segments  from  the  outer 
zone  pass  into  the  leaves  as  the  leaf  traces  and  the  gaps  thus  left  are  filled  up  by 
corresponding  segments  from  the  next  inner  zone." 

The  detailed  account  made  by  Miss  Shove  was  based  upon  a  moderate-sized 
specimen  from  Ceylon.  This  stem  is  described  as  being  somewhat  dorsiventral  in 
structure,  which  is  certainly  not  usual  in  Atigiopteris  and  may  perhaps  be  explained 
by  the  conditions  under  which  the  plant  was  growing.  I  found  Angiopteris  growing 
frequently  upon  steep  banks  and  it  is  quite  possible  that  plants  growing  in  such  a 
position  might  be  obliged  to  bend  upward,  in  which  case  a  somewhat  dorsiventral 
structure  would  be  developed.  Plants  growing  upon  level  ground,  so  far  as  my 
observations  go,  are  always  strictly  radial  in  structure. 

Miss  Shove  found  essentially  the  same  structure  as  that  described  by  Mettenius, 
except  that  she  states  that  the  leaf  traces  are  developed  exclusively  from  the  strands 
of  the  outer  zone,  while  Mettenius  states  that  strands  are  also  contributed  to  the 
leaf  trace  from  the  second  zone.    The  following  is  taken  from  her  paper  (Shove  I): 

"The  general  scheme  of  the  arrangement  of  the  vascular  tissue  in  Angiopteris 
is  almost  clearly  conceived  by  considering  it  in  connection  with  the  insertion  of  the 
leaves.  The  leaf  bases,  which  are  set  in  a  rough  spiral  on  the  stem,  shcnv  in  their 
lower  parts  a  meshed  segment  of  vascular  tissue  having  the  form  of  part  of  the  sur- 
face of  a  cylinder.  This  segment  passes  from  the  leaf  ba.se  into  the  outermost  zone 
of  the  stem,  uniting  right  and  left  with  the  strands  of  this  zone.  Then,  continuing 
in  an  obliquely  descending  direction,  it  passes  on  into  the  second  zone  and  so  on 
until  it  reaches  the  longitudinal  axis  of  the  stem,  where  it  unites  with  other  leaf- 
trace  bundles  and  loses  all  individuality." 

Miss  Shove  found  that  the  steles  in  the  stem  were  both  mesarch  and  endarch 
in  structure.  The  proto.xylem  is  found  in  groups  of  two  or  more  spiral  tracheids, 
some  of  them  at  the  periphery  and  some  in  the  center  of  the  stele.  The  number  of 
protoxylems  varies  with  the  size  of  the  stele,  the  larger  ones  usually  containing  five 
or  six  such  groups.  The  earliest  protoxylem  appears  at  the  periphery  of  the  stele. 
Protophloem  is  developed  upon  the  outer  side  of  the  stele  in  the  form  of  discontinu- 
ous, small,  thick-walled  elements,  which  Miss  Shove  regards  as  sieve  tubes.  This 
protophloem  does  not  occur  upon  the  inner  side  of  the  xylem.  A  remarkable  pecu- 
liarity of  the  bundle  is  the  fact  that  the  secondary  sieve  tubes  are  formed  outside  the 
protophloem  instead  of  within  it.  The  phloem  is  of  greater  breadth  on  the  outer 
side  of  the  stele  than  on  the  inner.  No  endodermis  could  be  detected  about  the 
steles  in  the  stem.  The  usual  absence  of  sclerenchyma  w^as  noted  for  the  stem.  Miss 
Shove  was  unable  to  determine  the  nature  of  the  apical  meristem  and  the  question 
still  remains  open,  whether  the  stem  grows  from  a  single  apical  cell  orfVom  a  group, 
such  as  is  found  in  the  larger  roots. 

It  appears  from  the  account  of  both  the  older  and  more  recent  investigators 
that  the  complicated  system  of  concentric  meshed  zones  in  the  adult  stem  oi  Angiop- 


202 


THE    MARATTIALES 


teris  is  really  built  up  of  leaf  traces,  the  so-called  "compensating  segment"  being 
nothing  more  than  the  lower  part  of  a  leaf  trace  which  higher  up  emerges  as  a  meshed 
segment  from  the  outer  zone  and  passes  into  the  base  of  the  leaf. 

The  structure  of  the  petiole  (fig.  182,  /f )  is  like  that  of  Maratti a,  except  that 
the  vascular  bundles  are  more  numerous  and  are  arranged  in  several  circles,  inclos- 
ing one  or  two  small  bundles  in  the  center.  A  cross-section  of  a  leaflet  (fig.  182,  B) 
shows  the  vascular  bundle  which  traverses  the  midrib  to  be  horseshoe-shape  in 
section,  having  a  central  mass  of  tracheids,  with  reticulate  or  scalariform  markings, 
and  surrounded  by  the  phloem,  largely  made  up  of  large  sieve  tubes,  but  having 
also  protophloem  cells  and  bast.  The  ground  tissue  is  composed  largely  of  paren- 
chyma, but  on  both  sides  below  the  epidermis  is  a  conspicuous  band  of  coUenchyma. 
In  the  larger  divisions  of  the  leaf  the  collenchyma,  as  in  Marattia,  is  replaced  by 
sclerenchyma.  The  structure  of  the  lamina  is  very  much  like  that  of  Dancra,  but 
the  palisade  parenchyma  is  even  better  developed. 

A  comparison  was  made  of  the  leaves  of  two  forms  (species  t)  of  Angiopteris, 
one  from  Australia,  the  other  from  Ceylon.  These  showed  several  notable  differ- 
ences.    The  leaflets  of  the  Ceylonese  specimens  were  thinner  and  sharply  serrate. 


Fig.  i%i.—Angiopte\ 

A.  Section  of  petiole  from  an  adult  sporophyte,  somewhat  reduced. 

B.  Section  of  a  leaflet,    co/,  collenchyma;   p,  palisade  tissue.     X14. 

C.  Part  of  sporophvll,  showing  the  sori.      X4. 

while  in  the  Australian  specimens  the  serrations  were  almost  wanting,  except  at  the 
tapering  apex  of  the  leaflet.  There  were  also  marked  anatomical  diff^erences.  In 
the  Australian  form  the  palisade  cells  are  very  much  elongated  and  are  separated 
from  the  epidermis  by  a  layer  of  colorless  hypodermal  cells,  and  the  spongy  meso- 
phyll  of  the  lower  part  of  the  leaf  is  decidedly  more  compact  than  in  the  form  from 
Ceylon.  In  the  latter,  the  palisade  cells  are  noticeably  shorter  and  abut  directly 
upon  the  epidermis.  Undoubtedly  the  diiTerences  in  the  anatomy  of  the  two  forms 
are  associated  with  the  diff^erence  between  the  moist,  tropical  climate  of  Ceylon  and 
the  drier  and  cooler  climate  of  Australia,  and  perhaps  do  not  necessarily  imply  that 
the  two  species  are  distinct,  although  it  is  highly  probable  that  such  is  the  case. 

The  roots  originate,  for  the  most  part,  in  the  inner  zones,  but  a  few  may  arise 
in  connection  with  the  bundles  of  the  outer  zones  and  must  necessarily  traverse  a 
very  large  amount  of  tissue  before  they  finally  emerge. 

Russow  (Russow  1)  described  two  sorts  of  roots — earth  roots  which  were 
branched  and  had  but  five  xylem  rays  completely  lignified  to  the  center  of  the  bun- 
dles, and  aerial  roots  which  were  much  larger  and  unbranchcd  and  had  twelve  to 


POROPUVTF 


203 


twenty  xylein  rays,  <)nl\'  the  outer  traelieids  lieiiii^  lii^iiitiecl.  In  tin-  |)lant  which  was 
examined  by  Miss  Shove  only  the  earth  roots  were  found,  and  these,  instead  of" 
having  only  five  xylenis  as  Russow  asserts,  had  from  ten  to  thirteen  and  the  xylem 
elements  were  entirely  lignified.  The  pioiiahilities  are  that  there  is  no  sharp  line 
to  be  drawn  between  the  aerial  roots  and  the  eaith  roots.  Figure  183  shows  a  sec- 
tion of  a  root  from  the  base  of  a  small  plant  from  Australia,  in  which  there  were 
fourteen  xylem  masses.  As  will  be  seen,  there  is  the  same  circle  of  large  mucilage 
ducts  and  the  tannin  cells  that  are  found  in  the  root  of  Mmattia,  which  it  very 
closely  resembles.  Root  hairs  are  nearly  or  quite  absent,  in  which  respect  these 
resemble  the  older  roots  of  other  Marattiacea^.  in  two  cases  Miss  Shove  found  a 
dichotomous  branching  of  the  root.  This,  while  probably  anomalous,  is  interesting, 
as  it  recalls  the  method  of  branching  in  the  roots  of  Op/iioglossiim. 

ARCHANGIOPTKRIS. 
The  genus  Archangioptnis.  with  a  single  species,  A.  henryi  Christ  and  Giesen- 
hagen,  is  at  present  known  onlv  from  a  single  locality  in  .southern  China.     Arrli- 
ano'iDl'tcris  in  habit  resembles  a  large  Dmur/i.      Vhv  leaves,  which  re.ich  a  length  of 


Fig.  ii-i,.—Angiopteris. 
A.  Section  of  a  large  root,     m,  mucilage  ducts.     X14. 
R.  Part  of  the  central  cylinder  of  the  root,    fw,  cndodcrmis.    X70. 

about  a  meter,  have  from  seven  to  twelve  leaflets,  much  like  those  o\' Dtnuvn  cUipticd, 
both  in  form  and  venation.  The  stalk  of  each  leaflet  is  swollen  in  a  manner  that 
suggests  the  nodular  swellings  in  the  petiole  of  Dan  a- a  elliptica  (fig.  184). 

The  only  account  of  the  structure  of  the  plant  is  that  ot  Gwynne-Vaughn 
(Gwynne-Vaughn  2),  but  as  he  had  only  a  fragment  of  a  stem  he  was  not  able  to 
make  a  complete  study  of  the  vascular  system.  To  judge  from  the  fragment  of  the 
stem  which  he  examined,  the  leaves  seem  to  be  arranged  spirally  and  the  stem 
is  probably  radial  in  structure.  The  general  structure  of  the  leaf  base  seems  to  be 
most  like  that  oi'  Kaiilfussia.  The  leaf  trace  consists  of  only  two  vascular  strands, 
which  divide  up  later  into  several  (eight  or  nine)  separate  strands,  arranged  at  the 
base  of  the  leaf  in  a  horseshoe  curve,  quite  like  that  of  Kaulfussia.  The  arrange- 
ment of  the  vascular  system  of  the  stipules  is  probably  the  same  as  in  the  other 
Marattiacea'.  The  structure  of  the  stem  is  also  apparently  very  much  like  that 
of  Kniilfiissia,  a  section  showing  only  one  circle  of  bundles  with  a  single  central 
strand.  The  root,  which  is  liki'  that  of  the  other  M.iiattiaciii'.  h;is  from  seven  to 
ten  xylem  rays. 


204 


THE    MARATTIALES 


MACROGLOSSUM. 

This  represents  a  new  genus  of  Marattiacese,  the  one  species  of  which,  M.  altdce 
Copeland,  has  recently  been  described  (Copeland  1).  It  is  a  large  fern  from  Borneo, 
and  is  evidently  related  to  Angtopteris,  from  which  it  differs  mainly  in  its  simply 
pinnate  leaves,  which  may  reach  a  length  of  about  3  meters  (see  Copeland  1,  plate  V). 


TISSUES  OF  THE  MARATTIACE^. 

There  are  often  present  upon  the  leaf  bases  of  the  Marattiaceae  peculiar  lenticel- 
like  structures  to  which  German  writers  have  given  the  name  "Staubgrubchen." 
These  arise  beneath  the  stomata,  and  form  small  cavities  whose  peripheral  cells 
become  detached  and  dried  up,  forming  a  dust-like  powder. 

Rod-shaped  bodies,  mainly  composed  of  cal- 
cium pectate,  are  of  common  occurrence  in  the 
intercellular  spaces  of  the  tissues  of  the  Marat- 
tiaceae. Siliceous  deposits  and  crystals  of  calcium 
oxalate  have  also  been  observed  in  Aiigiopteris 
(see  Bitter  1). 

The  elements  of  the  vascular  bundles  are  much 
like  those  in  the  bundles  of  the  ordinary  ferns.  The 
tracheary  tissue  is  composed  mainly  of  scalariform 
elements,  and  the  sieve  tubes  have  numerous  lateral 
sieve  plates,  like  those  of  the  other  ferns.  Hill  and 
Farmer  have  noted  a  slight  secondary  formation 
of  wood  in  Aiigiopteris,  somewhat  similar  to  but 
much  less  marked  than  that  in  the  stem  of  Botryr/i- 
iiivi  vngitiianiiDi  (see  Hill  I,  Farmer  3). 

THE  SIH)R01'HYLL  OF  THE  MARATTIACET,. 

The  Marattiaceae  differ  most  strikingly  from 
the  Ophioglossaceae  in  the  character  of  the  sporo- 
phylls.  In  all  of  the  living  Marattiaceae  the  sporan- 
gia or  synangia  are  borne  upon  the  lower  surface  I'lc  \'&^.--Arch^„gwi,u, 
of  the  leaves,  which  usually  are  not  at  all  different 
from  the  sterile  ones.  In  Dancea  (fig.  189)  the  sporophylls  are  decidedly  contracted 
and  the  very  large  synangia  almost  completely  cover  the  lower  surface  of  the  leaflets, 
but  in  the  other  genera  the  sporophyll  is  not  at  all  contracted  and  much  the  greater 
part  of  the  leaf  surface  is  free  (figs.  182,  184,  185,  188). 

Kaulfiissia  (fig.  1 88)  differs  most  from  the  other  genera,  the  very  peculiar  cir- 
cular or  rarely  oval  synangia  being  scattered  apparently  without  any  definite  order 
over  the  whole  lower  surface  of  the  leaf.  In  Dancea  the  elongated  synangia,  which 
lie  over  the  veins,  extending  from  the  midrib  nearly  to  the  margin  of  the  leaflet,  are 
crowded  so  that  they  leave  very  little  of  the  surface  free.  In  Marattia  and  Arigiop- 
teris  the  synangia  lie  over  the  veins  as  they  do  in  Datura,  but  they  are  very  much 
shorter  and  are  formed  near  the  margin  of  the  leaflet,  within  which  they  form  a 
single  line  which  occupies  only  a  very  small  part  of  the  leaf.  Archangiopteris,  except 
that  the  synangia  are  very  much  longer,  agrees  closely  with  Angioptens. 

No  proper  indusium  is  present  in  the  Marattiaceae,  although  very  commonly 
about  the  base  of  the  synangium  there  are  found  a  few  hairs  or  scales  which  have 
sometimes  been  considered  to  represent  an  indusium.  In  Dancra  there  is  a  growth 
of  tissue  between  the  elongated  synangia,  which  grows  up  into  a  sort  of  ridge,  the 


rvi  (after  Chri 
nd  Giesenhagen). 


205 


top  ot  which  is  txjiaiuliil  so  rliar  ir  o\iraiclits  the  s\iiany;ia.  I  his  ii(l<:;i-  in  section 
appears  T-shape.  Whether  this  growth  of  leaf  tissue  between  the  synangia  in 
Daiicea  is  to  be  considered  as  an  indusium  may  be  questioned.  It  appears  to  be 
very  simihir  in  structure  to  the  oblong  cavir\-  or  fovea,  within  which  is  sunk  the  nor 
very  ilissiniihir  s\nangiiini  u['  I  unirs  (Hg.   i  S9,  B). 


rHi;  Sl'OKANCIl'M  OV  THE  MAKATIIACi;  l- 

In  .Iiii^iiiptnis  and  Archangioptcris  there  are  formed  sejiarate  sjioiangia  not 
very  unhke  those  found  in  Bntrychiitm  or  Hclmnitltost(uli\s,  but  ui  all  the  otiier 
genera  the  sporangia  are  fused  into  a  synangium  which  might  be  compared  with 
the  spike  of  Ophioglossnui.  The  synangium  in  Danaa  sirn/^licifaha  may  reach  a 
length  of  over  3  centimeters  and  contain  upwaid  of  100  loculi.  I  he  first  study  of 
the  development  was  made  upon  Mardttia  h\  Lueissen  (Luersseii  3).  According 
to  his  statement,  the  differenti- 
ation of  the  synangium  begins 
while  the  leaf  is  still  very  small 
and  rolled  up  between  the  stip- 
ules. The  tissue  about  a  vein 
begins  to  develop  into  an  elevated 
cushion  following  the  vein.  Upon 
this  receptacle  there  are  devel- 
oped two  parallel  ridges  of  tissue, 
separated  by  a  cleft.  These  two 
ridges  later  grow  upward  and 
meet  above,  so  that  their  edges 
completely  close  up  the  cleft, 
which  no  longer  shows  from  the 
outside.  In  each  half  of  this  syn- 
angium, very  much  as  is  the  case 
in  the  sporangial  spike  of  Op/iio- 
glossum,  there  are  developed  sep- 
arate archesporial  groups  corre- 
sponding to  the  separate  cham- 
bers that  are  found  in  the  fully 
developed  synangium.  Luerssen 
states  that  the  whole  process  takes 
about  six  months  for  its  completion  (fig.  186). 

In  Angiopteris  (fig.  187)  the  development  of  the  sporangium  begins  at  a  much 
later  period,  when  the  leaf  is  almost  completely  developed.  Ihe  sporangia  here  are 
arranged  in  an  oblong  group  or  sorus,  which  corresponds  to  the  synangium  in  Marat- 
tia.  The  formation  of  the  sorus  begins,  according  to  Goebel,  as  an  oblong  depression 
above  a  young  vein,  and  about  this  depression  there  is  formed  a  circle  of  short  hairs 
which  are  sometimes  supposed  to  represent  an  indusium.  Two  ridges  corresponding 
to  those  found  in  the  young  synangium  of  Marattia  are  formed,  but  upon  these  the 
young  sporangia  develop  separately,  very  much  as  they  do  in  Botr\cliium. 

Goebel  states  that  the  archesporium  in  Aiigioptcris  can  be  traced  back  to  a 
single  hypodermal  cell.  This  cell  divides  repeatedly  but  apparently  without  any 
definite  order,  and  there  is  finally  formed  a  large  mass  of  sporogenous  tissue,  each 
cell  of  which  gives  rise  in  the  usual  way  to  four  spores.  The  cells  about  the  arche- 
sporium develop  the  tapetum.  Goebel  states  that  these  tapetal  cells  are  destroyed 
before  the  division  of  the  spore  mother  cells,  but  I  have  found  that  this  is  not  the 


Fig.  185.— A/araH/a  douglmii. 

A.  Leaf  from  a  young  sporophyte.    stj  stipules. 

B.  Leaflet  with  synangia.     X4. 

C.  Horizontal  section  of  a  synangium.     Xio. 


206 


THE   MARATTIALES 


case  and  that  the  tapctal  cells  persist  until  the  division  of  the  spores  is  complete. 
Bower  has  confirmed  this  statement  and  found  that  the  same  condition  of  things 
obtains  in  the  other  genera. 

The  most  complete  account  of  the  development  of  the  sporangium  is  that  of 
Bower  (Bower  6),  who  has  studied  the  development  in  all  of  the  genera  except 
Archangiopteris.  Except  for  the  difference  in  form,  there  is  no  essential  difference 
in  the  development  of  the  sporangia  in  Kaidfussia  and  Dana'a  from  that  found  in 
Marattta.  In  Datuea,  however,  the  individuality  of  the  loculi  of  the  synangium 
is  less  clear  than  in  the  other  genera.  Very  often  Bower  found  that  the  arche- 
sporium  became  divided  more  or  less  completely  by  parts  of  the  sterile  tissue,  some- 
what in  the  same  fashion  that  the  so-called  "trabeculae"  are  formed  in  I  sokes. 
In  DancEci,  moreover,  the  synangium  from  the  first  is  solid,  and  the  cleft  which  is 
present  in  the  young  synangium  of  Marattia  is  absent.  In  Kaulfussia  the  develop- 
ment of  the  synangium  differs  in  that  a  single  circular  ridge  is  formed  instead  of  the 


;  synangium  of  Marattia  fn 
jlder  synangium.    x,  the 


two  parallel  ones  found  in  Marattia,  and  the  loculi  or  chambers  of  the  synangium 
are  thus  arranged  in  a  circle  around  a  central  pit-like  depression.  Bower  states 
that  the  sporogenous  tissue  of  each  loculus  in  all  the  forms  he  examined  can  usually 
be  traced  to  a  single  mother  cell.  He  also  found  that  the  tapetum  always  arises 
from  the  cells  adjacent  to  the  archesporium,  and  that  normally  all  of  the  sporogenous 
tissue  develops  into  spores.  In  these  respects  the  Marattiacea?  closely  resemble 
H elmi uthostachys  and  Botrychiiim. 

In  Daiicea  and  Kaulfussia  there  is  no  mechanical  tissue  representing  the  annulus 
found  in  the  more  specialized  ferns.  The  dehiscence  of  the  sporangium  in  these 
forms  is  brought  about  merely  by  a  shrinking  of  the  cells  on  either  side  of  the  slit  by 
means  of  which  each  loculus  opens.  This  slit  is  very  short  in  Daua-a  and  may  finally 
appear  as  a  circular  pore,  but  it  is  not  essentially  different  from  the  more  elongated 
slit  found  in  Kaulfussia  and  Marattia.  In  the  latter  there  is  developed,  in  the  outer 
tissues  of  the  synangium,  mechanical  tissue  which  causes  the  two  halves  of  the 
synangium  to  separate,  very  much  like  the  two  covers  of  a  book,  and  the  elongated 
slit  from  each  loculus  opens  into  this  space  between  the  widely  separated  halves  of 
the  synangium. 


OLDliR    SrOKUl'llV 


207 


Ihe  ckliisccruu  of  tlic  iiidiv  idiial  loculi  is  affcctc-d  by  the  contractiiin  of  the 
tliiiiiici-wallcil  cells  siii  loumled  by  firmer  tissue.  The  spoian^iuiii  (A  ."ingiopteris  is 
undoLibtedly  a  more  speciahzed  structure  than  the  synaiifjium  of  tlie  other  Maratti- 
ace;e.  In  Angtoptcns  each  individual  sporangium  has  the  wall  on  the  outer  side 
much  thicker  than  that  on  the  inner  one,  and  the  superficial  cells  have  their  walls 
much  thickened.  The  inner  wall  is  sometimes  composed  of  but  one  layer  of  cells 
outside  of  the  tapetum,  but  more  commonly  there  are  one  or  two  layers  of  cells 
between  the  tapetum  and  the  epidermis.  Near  the  top  of  the  sporangium  on  its 
outer  side  there  is  a  transverse  band  of  cells  with  thicker  walls,  and  these  constitute 
a  rudimentary  annulus  very  much  like  that  found  in  the  Osmundaceae.  By  the 
contraction  of  this  thickened  annulus  the  longitudinal  slit  on  the  inner  face  of  the 
sporangium  is  made  to  open  widely  at  maturity.  1  he  number  of  s|iorcs  produced 
in  each  loculus,  according  to  Bower,  is  approximately  1,750  for  Dmian,  7.500  foi 
KauljnssKi,  2,500  for  Marattia,  and  1,450  for  Angiopteris. 

Which  type  of  sporangium  in  the  Marattiacea;  is  the  more  primitive  is  very 
difficult  to  say,  as  both  the  free  sporangium  like  that  of  Angioptrris  and  the  compact 

synangium  like  that  of  Manittia 
and  Daiicca  are  of  about  equal 
antiquity,  so  far  as  the  geological 
record  goes.  It  must  be  remem- 
bered that  the  living  Marattiace^e 
are  almost  certainly  merely  a  few 
isolated  fragments  of  a  once  large 
group,  and  it  is  by  no  means 
necessary  to  assume  that  the  spo- 
rangia of  the  living  forms  must 
necessarily  all  conform  to  a  com- 
mon primitive  type.  It  seems 
quite  as  likely  that  the  fVee  spo- 
rangia, like  those  of  Angtoptcns, 
may  have  originated  directly  from 
some  ancient  prototype  which 
resembled,  perhaps,  forms  like 
,  older  sporangiu,,,.     BoUychi  um  OY  H  Ami  nthostculivs, 

r.  the  annulus;  Mhcrorsistent  tapetum.    X75.  -'  -i         i  l  \ 

while  the  genera  with  the  solid 
synangium  like  Dtirura  may  have  come  from  forms  with  completely  united  spo- 
rangia like  Opiiioglossum. 

It  appears  from  a  study  of  the  most  ancient  ferns  that  these  bail  dinioipliic 
leaves,  the  sporophyll  probably  resembling  the  fertile  spikes  of  Botryihimii  or  the 
fertile  leaf  segments  of  Osmuiuia.  How  the  modern  Marattiace;e  originated  fVom 
forms  of  this  type  is  not  by  any  means  cieai.  i'he  development  in  Hclminthostaihys 
of  sterile  leaf-like  lobes  associated  with  the  sporangia  may  perhaps  afford  a  clew  to 
the  method  of  sterilization  by  which  the  sporangiophores  of  some  ty|ie  allied  to  the 
(^phioglossace;e  may  gradually  have  developed  sterile  green  leaf  segments,  bearing 
upon  their  lower  surface  sporangia  or  synangia  like  those  of  the  modern  Marattiace;c. 
These  sterile  segments  found  in  Hchniutlmstachys  are  occasionally  strikingly  leaf- 
like, and  as  the  groups  of  sporangia  in  Helvitnthostachys  are  sometimes  imited  into 
small  synangia,  the  development  of  similar  .synangia  upon  the  lower  suitaii  ol  siu  h 
green  sterile  segments  of  the  sporangiophore  is  quite  C()ncei\  abli-. 


Fio.  \%T.—Angiopterii. 
.A,  B.  sections  of  young  sporangia  (after  Goebel), 


Another  explanation  might  be  the  coalescence  of  tht 
of  a  sporophyll  like  that  found  in  the  Ophioglossace;e, 


fertile  a: 
bur  the 


the 


that  thi 


spo 


208 


THE    MARATTIALES 


langiophoie  in  all  of  the  living  Ophioglossaceae  is  adaxial,  while  in  the  Marattiaceae 
the  synangia  are  abaxial,  is  a  serious  objection  to  such  a  hypothesis;  and  the  most 
plausible  explanation  at  present  seems  to  be  that  of  a  progressive  sterilization  of 
part  of  the  sporophyll  itself  and  the  expansion  of  the  sterile  tissue  into  the  broad 
lamina  of  the  leaf  bearing  the  separated  sporangia  or  synangia  upon  its  lower  surface. 
It  must  be  admitted  that  the  difference  between  the  sporophylls  of  the  existing 
Marattiaceae  and  those  of  the  Ophioglossaceae  is  very  great,  and  the  leaves  of  the 
former,  superficially  at  least,  are  much  more  like  those  of  the  leptosporangiate  ferns; 
but  the  sporangia  themselves  are  very  similar  in  their  development  to  those  of  the 


Ophioglossaceae,  and  offer  no  obstacle  to  the  assumption  of  a  fairly  close  relationship 
between  the  Ophioglossaceae  and  the  Marattiaceae,  which  is  indicated  by  the  history 
of  the  development  of  the  gametophyte,  and  the  vegetative  organs  and  tissues  of  the 
sporophyte.  Perhaps  the  most  marked  difference  between  the  tissues  of  the  Marat- 
tiaceae and  the  Ophioglossaceae  is  the  prevalence  of  the  mucilage  ducts  in  the  tissues 
of  Marattiaceae,  but  these  arise  rather  late  in  the  history  of  the  sporophyte,  and  it  is 


Fig.  ii^.—Danxajamakensh. 
•     .  A.  Base  of  a  fertile  leaflet,  showing  synangia,  up.     X2. 

B.  Transverse  sections  of  three  synangia.     X12. 

C.  Horizontal  section  of  a  synangium. 

significant  that  they  are  less  developed  in  the  presumably  more  primitive  Kaulfiissia 
than  they  are  in  the  more  specialized  types  like  Angiopteris.  Another  difference  is 
the  development  of  sclerenchyma,  which  is  quite  absent  from  the  Ophioglossaceae; 
but  this  again  is  also  quite  absent  from  Kaulfussia,  which,  on  the  whole,  must  be 
considered  to  be  the  most  primitive  of  the  living  Marattiaceae  and  also  the  form 
which  most  closely  approaches  the  Ophioglossaceae. 


PARr  III.     THl^   ORIGIN    AND   RI:LA  llONSI  1 1  PS   ()!< 
1HI<;    PlUSl^ORANGIAT/i:. 

IIk  luspoiangiate  ferns  as  they  now  exist  represent  l)ut  a  fVu  isolatKl  hagnu  nts 
(ifwliat  in  earlier  geologic  time  was  presumably  a  very  nuicli  larger  and  more  (.(in- 
nected  gr()U|>.  As  the  geological  history  of  these  forms  is  very  far  from  clear  (this 
being  especially  true  of  the  Ophioglossaces),  we  are,  perforce,  dependent  niainl\- 
upon  a  comparative  study  of  the  few  existing  types  for  information  concerning  their 
relationships.  In  the  foregoing  pages  an  endeavor  has  been  made  to  trace  the  de- 
velopment of  these  forms,  both  in  their  gametophytic  and  early  sporophytic  stages, 
and  the  result  of  these  studies  has  been  to  confirm  the  belief  that  a  real  genetic 
relationship  exists  between  the  Marattiace^e  and  the  Ophioglossacex'. 

While  the  three  genera  of  the  Ophioglossace;e  differ  in  certain  particulars  from 
each  other,  there  is  no  question  as  to  their  being  comparatively  closely  related,  and 
the  same  is  true  of  the  different  genera  of  the  Marattiace;e,  although  perhaps  the 
differences  here  are  somewhat  greater  than  in  the  Ophioglossaceae. 

It  has  been  assumed  in  these  studies  that  the  sporophyte  of  the  ferns  is  the 
result  of  a  progressive  specialization  of  the  sporogonium  of  some  form  allied  to  the 
Bryophytes,  though  it  is  highly  improbable  that  any  of  the  existing  Bryophytes  are 
directly  related  to  this  progenitor  of  the  primitive  ferns.  No  attempt  will  be  made 
here  to  discuss  the  reasons  for  accepting  the  "antithetic"  theory  of  the  alternation 
of  generations,  rather  than  the  homologous  theory.  These  reasons  have  been  set 
forth  at  length  elsewhere. 

It  is  hopeless  to  expect  that  any  satisfactory  fossil  traces  will  be  found  of  these 
predecessors  of  the  true  ferns.  The  fern  type  is  exceedingly  ancient,  but  it  must 
have  been  preceded  by  simpler  forms  connecting  it  with  some  bryophytic  type. 
These  forms,  as  well  as  the  earlier  true  Pteridophytes,  were  almost  certainly  plants  of 
small  size  and  delicate  texture,  probably  not  very  unlike  some  of  the  small  and 
delicate  species  of  Ophioglossum.  Such  plants,  composed  entirely  of  soft,  pciish- 
able  tissues,  could  hardly  be  expected  to  leave  recognizable  fossil  traces,  and  their 
absence  from  the  ancient  Paleozoic  rocks  is  not  to  be  wondered  at. 

There  still  exist,  however,  among  the  Bryophytes,  certain  forms  which,  if  they 
are  not  directly  related  to  the  eusporangiate  ferns,  nevertheless  show  many  striking 
similarities  in  structure,  which  help  to  explain  at  least  what  may  very  well  have  been 
the  character  of  the  liverwort-like  ancestors  from  which  the  ferns  are  descended. 
Among  the  living  Bryophytes,  as  is  well  known,  an  interesting  series  of  types  may  be 
traced,  showing  the  gradual  increase  in  the  importance  of  the  neutral  generation — 
the  sporophyte — starting  as  little  more  than  a  mass  of  spores,  finally  by  a  progressive 
sterilization  of  what  wasoriginalh'  sporogenous  tissue,  and  an  accompanying  special- 
ization of  the  sterile  tissues  thus  formed,  attaining  a  condition  of  almost  complete 
independence.  The  importance  of  this  process  of  sterilization  of  potentially  sporo- 
genous tissue,  has  been  especially  clearly  expounded  in  the  works  of  Professor  Bower. 

In  two  classes,  the  true  mosses  or  Musci  and  the  horned  liverworts  or  Antho- 
cerotes,  the  sporophyte  continues  its  growth  for  several  months  and  develops  an 
elaborate  system  of  green,  assimilative  tissue,  quite  comparable  to  that  found  in 
the  vascular  plants.  The  spore-producing  function  is  correspondingly  subordinated 
and  the  spore  formation  is  delayed  until  a  late  period  in  the  life  of  the  sporophyte. 
14  2oy 


210 


ORIGIN    AND    RELATIONSHIPS    OF   THE    EUSPORANGIATAE 


The  large,  green  sporophyte,  however  (fig.  190,  A,  sp),  never  attains  complete  inde- 
pendence, as  no  proper  root  is  developed  and  it  is  dependent  for  its  water  supply 
upon  the  gametophyte. 

In  all  of  the  PZusporangiates,  the  embryo  is  much  later  in  developing  its  organs 
than  in  the  Leptosporangiates,  and  thus  resembles  the  Bryophytes;  moreover,  the 
embryo  reaches  a  very  much  larger  size  before  it  attains  its  independence.  Even 
after  the  young  sporophyte  has  developed   several  roots  and  leaves,  it  may  still 


Fig.  190. 
A.  Gametophyte  of  Anihotcros  sp.  with  the  large 
sporophyte,  5/>,  attached  to  it.  Upper  part 
of  spnropliyte  is  split  into  valves  which  allow 
the  escape  of  spores. 
B,  C.  Two  gametophvtes  of  Marattta  douglasii,  with 
attached  ^jiorophytc.  Sporophyte  emerges 
upon  tipper  side  of  gametophyte,  very  much 
as  in  Anthoicro^,  but  a  root,  r,  is  developed 
which  penetrates  lower  side  of  gametophyte 
and  connects  the  young  sporophyte  with  the 
earth,  g,  gametophyte;  jp,  sporophyte; 
/,  first  leaf;  r,  primary  root. 


maintain  its  connection  with  the  gametophyte  and  be  to  a  certain  extent  dependent 
upon  it  in  a  way  which  forcibly  recalls  the  relation  of  gametophyte  and  sporophyte 
in  the  mosses.  This  condition,  which  furnishes  a  very  strong  argument  in  favor  of 
the  primitive  nature  of  the  Eusporangiates  when  compared  with  the  Leptosporan- 
giates, is  especially  pronounced  among  the  Ophioglossace^e,  where  it  may  even  go  so 
far  that  spores  are  developed  before  the  connection  of  gametophyte  and  sporophyte 
is  finally  sundered. 

In  the  true  mosses  the  sporophyte  is  exceedingly  specialized  and  shows  but  a 
very  remote  resemblance  to  that  of  the  Pteridophytes.     In  Aiithoccros,  however,  the 


Fig.  191. 

Diagrams  which  show  the  similarity  in  form  of  the  very 
young  sporophyte  in  AnthoceroStA^  and  Ophioglossiini^ 
B.  In  the  former  the  upper  portion  becomes  an  elong- 
ated capsule  within  which  spores  are  produced.  The 
shaded  portion  shows  layer  of  sporogenous  tissue  sur- 
rounding central  sterile  tissue  or  columella.  The 
zone,  m,  between  capsule  and  foot,  /,  is  composed  of 
meristematic  tissue.  In  Ophioghsmm  the  upper  part 
of  the  young  sporophyte  forms  the  primary  leaf,  or 
cotyledon,  cot,  which  is  not  sporogenous.  The  colum- 
ella of  Anihoccros  is  replaced  by  the  axial  vascular 
bundle,  v.b.  At  the  junction  of  the  cotyledon  and 
foot  arises  the  primary  root,  r,  which  finally  penetrates 
the  foot  and  enters  the  ground. 


mosl  highly  developed  of  the  horned  liverworts,  there  are  a  number  of  very  significant 
structural  details  that  are  very  strongly  reminiscent  of  the  young  sporophyte  of 
Oph'toghssum  moluccanum.  In  both  of  these  forms  the  young  embryo  has  a  very 
large  foot  and  a  conical  upper  region  (fig.  191).  This  upper  portion  in  Ophioglossum 
develops  into  the  cotyledon;  in  Anthoceros,  into  the  spore-bearing  part  of  the  sporo- 
phyte. Above  the  foot  in  Anthoceros  there  is  developed  a  zone  of  meristematic 
tissue  by  means  of  which  new  cells  are  added  to  the  base  of  the  growing  spore- 


ORIGIN    AND    RELATIONSHIl'S    OK   THE    EUSPORANGIATAE 


211 


phyte,  and  in  Op/iioglossum  much  the  same  thing  occurs  in  the  cotyledon,  although 
at  first  this  grows  from  a  single  apical  cell.  It  is  probable  that  in  the  ancestors  of  the 
Ophioglossace.ne  this  upper  conical  portion  of  the  embryo  was  developed  directly 
into  a  spore-bearing  organ.  There  is,  however,  a  marked  difference  which  soon 
appears,  viz,  the  development  of  a  true  root  in  Op/iioglossutii.  This  root,  pushing 
down  through  the  foot,  penetrates  the  lower  side  of  the  gametophyte  and  places  the 
young  sporo|)hyte  directly  into  communication  with  the  water  supply  from  the  earth, 
and  thus  the  latter  becomes  entirely  independent.  Were  the  large  sporophyte  of 
Antlioceros  to  develop  a  similar  root  from  the  basal  meristem,  it  also  would  become 
entirely  self-supporting.  Indeed,  so  marked  are  the  resemblances  in  the  early  stage  of 
development  that  they  make  the  inference  almost  irresistible  that  the  Ophioglossaceae 
must  have  descended  from  some  simpler  forms  whose  sporophyte  bore  a  strong 
resemblance  to  Antlioceros.  This  "pro-Ophioglossum,"  if  we  may  call  it  so,  pre- 
sumably produced  spores  upon  the  first  leaf,  instead  of  its  being  a  sterile  cotyle- 
don as  in  the  existing  forms.     From  a  study  of  the  development  of  the  sporophyte 


192.- 


Comparison  of  sexual  organs  in  Anthoccrotacca;  and  Marallia. 

of  the  thallus  of  Anihoccros  pearsoni  Howe,  showing  an  anthcridium  mother  cell, 


A.  Longiludin; 

witli  the  superimposed  cover  cell  {d). 

B.  An  older  anthcridium  within  a  cavity  covered  by  a  double  layer  of  cover  cells. 

C.  Young  archegonium  of  Xtegaceros  IjiboiUnsii  Campbell,  a  form  closely  related  to  Anihoceios. 

D.  Sections  of  young  antheridia  of  Marattia  tiouglasii  Baker.    The  inner  cell  divides  at  once  into  the  sperm 

cells,  and  the  cover  remains  single-layered,    dy  the  cover. 

E.  Young  archegonia  of  Mara/f/fl  rfoHjj/ajiV.    I,  the  basal  cells  of  the  archegonium;  </,  neck. 

in  O.  moluccaniim,  it  may  be  inferred  that  this  ancestral  form  had  no  stem,  but 
consisted  simply  of  this  spore-bearing  leaf  and  a  root.  The  sporangia  were  presum- 
ably simpler  than  in  the  existing  forms  of  Ophioglossiiui,  and  perhaps  intermediate 
in  character  between  such  sporangia  as  those  of  the  smaller  species  of  Opiiioglossutn 
and  the  imperfectly  segregated  spore  groups  which  occur  in  the  Anthocerotes. 

Not  only  does  the  sporophyte  of  Antlioceros  show  important  resemblances  to 
that  yif  Opliioglossnni,  but  the  development  of  the  sexual  organs  also  shows  striking 
analogies.  The  archegonium,  unlike  that  of  other  Bryophytes,  is  sunk  below  the 
surface  in  much  the  same  fashion  as  that  of  the  eusporangiate  ferns,  and  the  short 
neck  of  the  archegonium  in  the  latter  is  probably  to  be  compared  to  the  four  terminal 
neck  cells  which  may  occur  in  the  Anthocerotes  (fig.  192).  The  endogenous  anther- 
idia of  the  Anthocerotes  also  may  perhaps  be  compared  to  *he  sunken  antheridia  of 
the  eusporangiate  ferns,  and  in  their  early  stages  the  resemblances  are  very  close. 


212  ORIGIN    AND    RELATIONSHIPS    OF    THE    EUSPORANGIATAE 

Ihe  most  marked  difference  in  the  character  of  the  reproductive  organs  is  the 
spermatozoid.  The  spermatozoids  in  the  luisporangiates,  especially  in  Ophio- 
glossum,  are  very  large  and  possess  numerous  cilia,  while  in  Anthoceros  they  are 
minute  and  have  but  two  cilia,  like  the  other  Bryophytes.  This  is  perhaps  the  strong- 
est reason  for  assuming  that  there  is  not  a  direct  connection  between  the  Anthoce- 
rotes  and  the  Ophioglossaceae;  but  both  gametophyte  and  sporophyte  have  so  many 
points  in  common  that  it  may  be  pretty  safely  assumed  that  the  progenitors  of  the 
Ophioglossaceae  were  not  very  different,  in  appearance  at  least,  from  the  living //«- 
thoceros.  Whether  the  differences  in  the  spermatozoid  are  secondary  remains  to  be 
seen,  but  in  view  of  the  extraordinary  constancy  of  the  form  of  the  spermatozoids 
in  all  of  the  main  groups  of  the  Archegoniates,  one  would  certainly  expect  that  large 
multiciliate  spermatozoids  would  be  found  in  the  ancestors  of  the  Kusporangiates, 
supposing  these  should  ever  be  discovered. 

There  is  no  question  that  the  subterranean  prothallium  of  the  Ophioglossaceae 
is  a  secondary  condition,  derived  from  some  green  gametophyte,  probably  very  much 
like  that  of  the  Marattiaceae.  Not  only  has  the  chlorophyll  been  lost,  but  in  Op/iio- 
glossum  and  Helminthostachys  the  dorsiventral  form  of  the  gametophyte  has  been 
replaced  by  a  radially  symmetrical  thallus.  While  this  may  be  partially  explained 
as  the  result  of  the  absence  of  light,  it  must  be  remembered  that  the  equally  sub- 
terranean prothallium  of  Botrychiiim  is  dorsiventral,  although  the  reproductive 
organs  are  borne  upon  the  dorsal  surface  and  not  upon  the  ventral  one,  as  they  are 
in  most  ferns.  Whether  this  position  of  the  reproductive  organs  is  the  result  of  the 
conditions  of  growth  or  whether  it  indicates  that  the  green  gametophyte  from  which 
this  saprophytic  underground  form  is  descended  also  bore  the  reproductive  organs 
dorsally,  as  most  liverworts  do,  can  only  be  conjectured.  In  the  Marattiaceae 
antheridia  are  not  uncommon  upon  the  dorsal  surface,  and  according  to  Jonkmann 
archegonia  also  may  occur  dorsally.  Whether  this  is  normal  or  is  the  result  of  unusual 
light  conditions  was  apparently  not  investigated.  The  formation  of  archegonia  in  the 
ordinary  ferns  may  be  induced  upon  the  dorsal  side  of  the  prothallium,  provided 
it  is  illuminated  from  below.  If  the  illumination  is  equal  on  both  sides,  archegonia 
will  develop  both  on  the  ventral  and  dorsal  surface. 

Of  the  investigated  species  of  Ophioglossiim,  0.  moluccanum  and  the  nearly 
related  and  perhaps  identical  O.  penduncnlositm  probably  represent  the  most  primi- 
tive type.  In  these  species  there  may  be  a  feeble  development  of  chlorophyll  in  the 
gametophyte  under  certain  conditions  and  the  saprophytic  habit  is  much  less  pro- 
nounced than  it  is  in  the  other  species  of  Ophioglossiim  and  Botrychium. 

The  development  of  an  endotropic  mycorrhiza  in  the  prothallium  of  the 
Marattiaceae  is  an  interesting  suggestion  as  to  the  probable  beginning  of  the  sapro- 
phytic habit  which  characterizes  the  gametophyte  of  the  Ophioglossaceae.  There 
seems  to  be  good  reason  to  suppose  that  the  peculiar  type  of  symbiosis,  which  is 
developed  so  highly  in  the  Ophioglossaceae,  began  by  the  development  of  a  fungus 
associate  in  some  green  gametophyte  like  that  of  the  Marattiaceae. 

The  reproductive  organs  of  the  C^phioglossaceas  and  Marattiaceae  are  very 
similar  indeed.  It  is  probable  that  the  short-necked  archegonium  found  in  the 
Marattiaceae  and  in  Ophioglossiim  is  more  primitive  than  the  long-necked  arche- 
gonium of  Botrychium  or  Helminthostachys.  This  conclusion  is  based  upon  the 
assumption  that  the  four-necked  archegonium  of  the  ferns  is  a  development  of  the 
four  terminal  cells  in  the  neck  of  the  Bryophyte  archegonium,  Anthoceros  most 
nearly  approaching  this  hypothetical  ancestral  type.  This  being  the  case,  the  forms 
with  the  shortest  neck  would  most  nearly  resemble  this  assumed  ancestral  type. 


ORIGIN    AND    RELATIONSHII'S    Ol-    THK     KUSPORANGIATAE  213 

The  question  of  tlif  canal  cells  is  a  |ni/./ling  one.  In  the  Maiattiacea-,  with  the 
exception  of  D/ui.ni,  two  neck  canal  cills,  or  at  any  rate  two  nuclei,  are  present  and 
the  ventral  canal  cell  is  consjiicuoiis.  In  Dainra,  however,  the  canal  cells  are  very 
much  less  perfectly  developed,  the  ventral  canal  cells  especially  heing  exceedingly 
difHcult  to  demonstrate.  In  the  latter  respect  Daiuva  shows  a  remarkable  resem- 
blance to  the  ()phioglossace:e,  especially  to  Ophioglossuni,  where  the  ventral  canal 
cell  is  equally  difficult  to  demonstrate.  Ihis  apparent  degeneration  of  the  ventral 
canal  cell  is  probably  secondary,  as  all  of  the  Bryophytes  and  the  other  Pteridophytes 
have  the  ventral  canal  cell  ccjnspicuous. 

The  antheridium  in  all  of  the  Marattiace;e  is  almost  exactly  like  that  of  Op  hi  o- 
glossum,  while  Botrychnim  and  Helminthostachys  differ  in  having  the  outer  wall  of 
the  antheridium  more  or  less  completely  two-layered.  If  the  antheridium  is  derived 
from  a  type  like  that  of  Anthoceros  (fig.  192),  where  the  antheridial  cavity  is  covered 
by  a  double  layer  of  cells,  it  would  seem  that  Botrychiiim  and  Helminthostachys  are 
more  primitive  than  Ophioglossuni  or  the  Marattiace;e  in  this  respect. 

Of  the  Eusporangiates,  there  is  no  question  that  the  type  of  embryo  found  in 
Ophioglossum  moliiccaniim  comes  the  nearest  to  the  assumed  ancestral  form.  This 
hypothetical  pro-fern  may  be  assumed  to  have  developed  simply  a  spore-bearing 
organ  or  sporangiophore,  perhaps  more  or  less  leaf-like,  and  a  root  developed  from 
the  inner  part  of  the  massive  foot  in  the  same  way  that  the  root  actually  does  develop 
in  the  embryo  of  the  Marattiaceae  and  Ophioglossum  mohucanum.  Except  that  the 
cotyledon  of  O.  moluccanitm  is  sterile,  the  young  sporophyte  in  this  species  is  actually 
like  this  hypothetical  type,  viz,  it  is  composed  simply  of  root  and  leaf.  It  is  probable 
that  the  fertile  spike  of  Ophioglossum  is  not  unlike  the  primitive  sporangiophore, 
and  the  ancestral  form  presumably  developed  such  a  spike-like  sporangiophore  from 
the  first,  the  sterile  lamina  being  a  secondary  structure  arising  perhaps  from  a  basal 
meristem,  like  that  found  in  the  sporophyte  of  Anthoceros.  The  early  development 
of  the  spores  in  the  Ophioglossaceae  is  a  further  indication  of  their  primitive  nature. 

The  monophyllous  condition  which  prevails  among  the  Ophioglossacea:'  must 
also  be  regarded  not  as  a  secondary  condition  but  as  a  primitive  one,  and  a  study  of 
the  development  of  the  sporophyte  lends  no  support  to  the  theory  that  we  have  to 
do  with  a  reduced  strobilus.  Of  the  Marattiaceae,  Kaulfussia  normally  approaches 
the  monophyllous  condition  more  closely  than  any  other  genus.  The  older  plants, 
as  a  rule,  have  only  two  or  three  leaves  expanded  at  one  time  and  there  may  fre- 
quently be  but  one.  In  strong  contrast  with  this  is  the  dense  crown  of  leaves  found 
in  Marattia  and  Angioptciis,  although  even  in  these  forms  the  number  of  leaves  is 
less  than  it  is  in  the  majority  of  leptosporangiate  ferns.  The  tendency  to  the  mono- 
phyllous condition  is  shown  in  the  younger  plants  of  Marattia,  developed  from  the 
buds  on  the  old  leaf  bases,  where,  as  a  rule,  only  one  leaf  is  expanded  at  a  time. 

The  young  sporophyte  of  O.  molurranutti  has  ?io  stem.  Without  exception,  for 
a  considerable  time  at  least,  the  vascular  system  of  the  sporophyte  is  composed 
exclusively  of  tissue  belonging  to  the  leaves  and  roots,  the  stem  apex  playing  no 
part  in  the  building  up  of  the  vascular  skeleton.  The  theory  that  there  is  a  special 
stele  belonging  to  the  stem,  of  which  the  leaf  traces  and  the  root  traces  are  sub- 
sidiary structures,  is  not  borne  out  by  a  detailed  study  of  the  evolution  of  the  vascular 
system  in  either  the  Marattiace.e  or  Ophioglossacc;c.  In  all  of  these  that  I  have 
examined  the  vascular  system  begins  as  a  single  strand  common  to  the  primary 
leaf  (or  cotyledon)  and  the  primary  root,  and  the  more  complicated  vascular  system 
of  the  older  stem  for  a  very  consitlerable  period  is  built  up  exclusiveh'  b\-  additions 
(it  new   liaf   traces  or  root  steles.      1  his  condition  is  permanent  111   rlu-  ( )phioglos- 


214  ORIGIN    AND    RELATIONSHIPS    OF    THE    EUSPORANGIATAE 

saceae.  In  the  Marattiaceae  small  cauline  bundles  (commissural  bundles)  may  be 
developed  at  later  stages,  but  these  are  insignificant  compared  with  the  complex  of 
united  leaf  traces. 

The  antithetic  theory  of  alternation  implies  that  the  sporophylls  are  older 
structures  than  the  sterile  leaves,  and  those  ferns  in  which  the  sporogenous  function 
of  the  sporophylls  is  most  pronounced  may  be  assumed,  other  things  being  equal, 
to  be  the  most  primitive.  In  this  respect,  as  well  as  in  the  usually  monophyllous 
condition,  the  Ophioglossaceae  are  distinctly  more  primitive  than  the  Marattiaceae. 
The  sporangiophore  or  fertile  leaf  segment  is  a  practically  independent  structure, 
being  differentiated  at  an  extremely  early  period  in  the  development  of  the  leaf. 
In  the  Marattiaceae  the  sporangia  are  subordinate  and  the  leaves  upon  which  they 
are  borne  usually  differ  in  no  respect  from  the  sterile  leaves.  The  most  marked 
exception  to  this  is  Da?icra,  in  which  the  sporophylls  differ  decidedly  from  the  sterile 
leaves  and  the  synangia  are  much  larger  than  those  of  the  other  genera,  although 
the  leaves  themselves  are  usually  smaller. 

Bower  thinks  that  the  circular  synangium  of  Kaulfiissia  is  the  most  primitive 
type  among  the  existing  Marattiaceae,  but  there  is  some  reason  to  doubt  the  sound- 
ness of  this  conclusion;  at  any  rate,  on  theoretical  grounds,  the  large  synangia  and 
contracted  sporophylls  of  Dancca  must  be  assumed  to  be  more  primitive  than  the 
type  of  leaf  found  in  Kaiilfussia.  In  regard  to  the  character  of  the  sporophylls, 
therefore,  none  of  the  living  Marattiaceae  can  be  regarded  as  being  very  primitive. 
All  of  the  oldest  fern  fossils  show  the  sporangia  to  be  borne  upon  special  leaves  or 
leaf  segments,  in  which  the  lamina  is  nearly  or  quite  absent  (Scott  1,  Bower  9). 
In  this  respect,  therefore,  these  ancient  fossil  ferns  were  more  like  the  Ophiogloss- 
aceae  than  like  the  Marattiaceae,  although  their  sporangia  came  nearer  to  the  type 
of  Marattiaceae.  It  is  by  no  means  impossible  that  these  oldest  ferns,  e.  g.,  the 
Botryopterideae,  were  related  to  the  Ophioglossaceae. 

The  single  apical  cell  found  in  the  stem  apex  throughout  the  life  of  the  sporo- 
phyte  in  Ophioglossum  is  probably  a  more  primitive  condition  than  the  group  of 
cells  found  in  Angwpteris.  It  still  remains  to  be  seen  whether  the  single  apical  cell 
found  in  the  other  Marattiaceae  in  their  early  stages  is  persistent  throughout  life  or 
is  replaced,  as  in  the  roots,  by  a  group  of  initial  cells. 

The  single  axial  strand  of  collateral  structure  throughout  cotyledon  and  loot 
may  be  taken  as  the  starting  point  for  two  types  of  vascular  skeleton  which  have 
arisen  from  it.  The  first  is  that  of  Ophioglossum,  where,  with  the  development  of 
the  new  leaves,  there  is  built  up  the  wide-meshed  cylindrical  network  or  dictyostele, 
composed  of  single  collateral  leaf  traces.  A  further  development  of  the  same  type 
results  in  the  much  more  complicated  dictyosteles  of  the  Marattiaceae,  where,  more- 
over, the  collateral  bundles  are  replaced  by  concentric  ones.  This  greater  com- 
plexity is  due  primarily  to  the  much  larger  leaves  of  the  Marattiaceae,  in  which  the 
leaf  traces  are  compound.  In  the  earlier  stages  of  these  forms,  however,  we  have 
seen  that  the  young  leaf  traces  are  single  and  the  structure  of  the  vascular  skeleton 
exactly  as  it  is  in  Ophioglossum.  Of  the  Marattiaceae,  Kaulfussia  more  nearly 
retains  this  primitive  condition  than  the  other  genera  and  next  to  this  comes  Dancea, 
while  further  removed  from  the  primitive  type  is  the  exceedingly  complex  skeleton 
found  in  the  massive  stem  of  Angiopteris.  The  concentric  bundles,  characteristic 
of  the  Marattiaceae,  are  presumably  of  secondary  origin  and  we  find  that  in  the 
early  bundles,  especially  of  Danaa,  a  true  collateral  structure  is  present. 

The  second  type  of  skeleton  is  that  found  in  Botrychium  and  Helmmthostachys. 
This  is  a  solid,  hollow  cylinder  with  inconspicuous  leaf  gaps,  resulting  from  the 
union  of  the  broad  leaf  traces,  which  fuse  completely  to  form  this  hollow  stele.    That 


ORIGIN    AND    RELATIONSHIPS    OF   THE    EUSPORANGIATAi:  215 

the  cyliinlriiiil  Inindlc,  or  siphonostele,  is  not  due  to  the  formation  of"  :i  pitli  within 
a  protostele  is  clearly  shown  hy  the  study  of  the  developmcnt|^of  the  hundle  in  the 
young  sporophyte  of  lioirycliiiim,  where  it  can  easily  be  seen  that  the  component 
bundles  are  separate  at  first,  and  that  the  pith,  so-called,  of  the  siphonostele  is  merely 
a  portion  of  the  ground  tissue  that  is  included  between  them,  and  which  later  be- 
comes entirely  separated  from  the  cortical  tissue.  A  similar  condition  of  things  may 
be  found  in  tracing  the  development  of  the  vascular  cylinder  in  the  young  stem  of 
Helminthostachys.  The  development  of  the  young  bundles  in  Angioptcns  is  more 
like  Botrychimn  than  Ophioglossuni,  and  this,  in  connection  with  the  separate 
sporangia  that  occur  in  Augiopteris,  suggests  that  perhaps  the  type  ot  the  Marat- 
tiaceae  represented  by  Augiopteris  may  have  originated  independently  from  forms 
like  Helminthostachys,  instead  of  having  had  the  same  origin  as  tiiose  forms  in 
which  true  synangia  are  developed. 

The  essential  similarity  of  the  leaf  structures  throughout  the  Ophioglossacea' 
is  sufficiently  clear,  antl  the  steps  in  the  increasing  complexity  of  the  sporophyll  can 
be  easily  traced  in  existing  forms,  ranging  from  the  undivided  fertile  and  sterile 
segments  of  Ophioglossiim  to  the  decompound  leaves  and  much-branched  panicle 
oi  Botrychium.  Helminthostachys  is  much  the  most  aberrant  of  the  Ophioglossaceae 
and  in  many  respects  shows  a  marked  resemblance  to  the  Marattiaceie.  The  form 
and  venation  of  the  leaves  strongly  recall  Dana-a  or  Angiopteris,  except  that  the 
leaves  are  not  pinnately  divided,  in  which  respect  they  closely  resemble  Botrychium. 
It  must  be  remembered,  however,  that  the  ternate  form  of  leaf  characteristic  of 
Botrychium  and  Helminthostachys  is  very  generally  met  with  in  the  early  stages  of 
the  sporophyte  in  the  Marattiaceae.  The  anatomy  of  the  leaf  in  Helminthostachys 
very  closely  resembles  that  of  the  Marattiacere,  there  being  a  well-developed  palisade 
layer  in  the  mesophyll,  a  character  which  is  either  wanting  entirely  or  very  imper- 
fectly developed  in  Botrychium. 

The  leaves  of  the  Marattiaceae,  except  in  Kaulfussia,  in  their  form  and  in  the 
circinate  coiling  of  the  young  leaves,  suggest  a  relationship  with  the  leptosporangi- 
ate  ferns  rather  than  with  the  Ophioglossaceae.  However,  the  larger  species  of 
Botrychium  and  Helminthostachys  show  an  approach  to  this  circinate  form  of  the 
young  leaf,  this  being  especially  conspicuous  in  the  young  sporophylls  oi  Botrychium 
virginianum.  With  the  exception  of  Kaulfussia,  the  general  form  and  venation 
are  alike  in  all  the  Marattiace;e  and  have  their  nearest  analogy  in  Helminthostachys. 
There  seems  no  reason  to  assume  that  the  stipular  sheath  in  the  Marattiaceae  is  dif- 
ferent in  its  nature  from  that  of  the  Ophioglossaceae,  especially  Helminthostachys 
and  Botrychium.  The  ternate  form  of  the  leaf  may  be  persistent  in  Kaulfussia, 
where,  however,  the  venation  is  more  like  that  of  Ophioglossum.  Whether  this 
occurrence  of  both  reticulate  and  pinnate  venation  in  the  two  families  is  a  case  of 
parallel  development,  or  whether  it  indicates  the  connection  of  the  families  at  dif- 
ferent points,  it  is  at  present  impossible  to  say. 

In  the  structure  of  the  roots  the  Marattiaceae  find  their  nearest  ally  in  Hel- 
minthostachys, where  the  number  of  the  xylem  rays,  four  to  seven,  equals  that  of 
Kaulfussia,  which  has  the  simplest  structure  among  the  Marattiacea%  and,  as  we 
have  seen,  probably  on  the  whole  is  most  nearly  related  to  them.  Helminthostachys 
also  resembles  the  Marattiacex  in  the  character  of  the  apical  growth  of  the  root, 
where,  although  there  is  a  single  apical  cell,  such  as  occurs  in  the  young  roots  of  the 
Marattiacea-,  its  form  is  more  like  that  of  the  Marattiaceae  than  it  is  like  that  of 
Botrychium.  The  endophytc  which  occurs  in  the  older  roots  of  the  Ophioglossacea',  as 
well  as  in  the  primary  one,  I  have  not  fouml  in  the  older  roots  of  the  Marattiaceae,  at 
least  notas  a  regularthing,  although  it  seems  to  be  always  present  in  the  primary  root. 


216  ORIGIN    AND    RELATIONSHIPS    OF    THE    EUSPORANGIATAE 

The  Ophioglossaceae  and  Marattiaceae  are  alike  in  the  absence  of  any  mechan- 
ical tissues  in  the  cortex  of  the  stem.  Sclerenchyma,  which  is  well  developed  in 
the  leaves  of  most  of  the  Marattiaceae,  seems  to  be  entirely  wanting  in  all  of  the 
Ophioglossaceae,  but  the  coUenchyma  which  replaces  sclerenchyma  in  certain 
organs  of  the  Marattiaceae,  and  is  the  only  form  of  mechanical  tissue  in  Kaidfttssia, 
is  occasionally  found  in  the  Ophioglossaceae.  A  notable  case  of  this  is  the  broad  and 
very  conspicuous  zone  of  coUenchyma  surrounding  the  root  bundle  in  Ophioglossiim 
palmatum.  The  mucilage  ducts  so  characteristic  of  Marattiaceae  are  apparently 
quite  wanting  in  all  of  the  Ophioglossaceae,  and  the  tannin  sacs  which  are  a  nearly 
constant  feature  in  the  Marattiaceae  are  absent  in  Botrychium  and  Ophioglossum, 
but  occur  in  Helmmthostachys. 

In  the  general  structure  of  the  vascular  bundles  there  are  important  resem- 
blances. In  both  families  the  first-formed  tracheids  in  the  young  sporophyte  are 
all  of  the  short,  reticulate  form,  and  this  is  retained  permanently  in  Ophioglossum, 
but  is  replaced  later  by  pitted  tracheids  in  Helminthostachys  and  Botrychium. 
Hchninthostachys  alone  among  the  Ophioglossaceae  shows  spiral  protoxylem  ele- 
ments like  those  found  in  the  later  bundles  of  the  Marattiaceae. 

It  is  probable  that  the  collateral  bundles  of  Ophioglossum  represent  the  prim- 
itive type  from  which  the  concentric  type  found  in  the  Marattiaceae  has  been  derived. 
In  Botrychium  and  Helminthostachys,  while  the  collateral  type  of  bundle  is  found 
in  the  stem,  in  the  petioles  the  bundles  are  concentric,  as  they  are  in  the  Marattiaceae. 
The  collateral  type  of  bundle  reappears  again  in  the  early  stages  of  the  sporophyte 
in  Dancea. 

Angiopteris,  which  is  probably  the  most  specialized  of  the  living  Marattiaceae, 
has  concentric  bundles  only. 


C()N(-LUSION. 

W'liilf  tin-  nioiv  specialized  Maiattiacea',  like  Muruttui  and  Angioptcris, 
apparently  differ  very  much  from  the  Ophioglossacea-,  it  appears  from  a  study  of 
the  development  of  these  forms,  as  well  as  that  of  the  simpler  and  presumably  more 
primitive  genera  Dana:a  and  Kaulfussiti,  that  the  most  conspicuous  differences  are 
of  secondary  rather  than  of  primary  importance,  and  the  conclusion  is  justified  that 
the  two  families  of  the  I'^usporangiata-  really  arose  from  the  same  primitive  stock. 
Of  the  Ophioglossaceae,  Helmmthostachys  is  undoubtedly  the  form  which,  nn  rlu- 
whole,  comes  nearest  to  the  Marattiacea;,  although  Ophioglossinn  is  more  like  them 
in  the  character  of  the  reproductive  organs  and  in  the  vascular  skeleton  of  the 
sporophyte.  Op/iioglossiirn  also  recalls  Kaiilfiissm  in  the  form  and  venation  of 
its  leaves. 

While  the  green  gametophyte  in  the  Marattiacea'  is  undoubtedly  a  more 
primitive  structure  than  the  saprophytic  prothallium  of  the  Ophioglossaceze,  the 
sporophyte  of  the  latter  is  certainly  a  more  primitive  one  than  that  of  the  Marat- 
tiacea.  The  monophyllous  condition,  the  early  development  of  the  sporangia,  and 
the  fact  that  the  whole  of  the  sporangiophore  is  spore-bearing,  all  point  to  this. 

The  way  in  which  the  sporophyll  of  the  Marattiacea  has  been  derived  from  a 
type  like  that  of  the  Ophioglossacea  is  not  clear,  and  it  is  by  no  means  certain  that 
all  of  the  Marattiacea  have  been  developed  in  the  same  way.  The  occurrence  of 
fossil  forms  with  sporangia  of  the  marattiaceous  type  grouped  together — much  like 
the  sporangia  of  Botrychiiim  orOsmimda — suggests  that  such  a  condition  might  have 
been  preliminary  to  the  separation  of  the  sporangia  by  the  development  of  sterile 
green  tissue  in  the  sporangiophore,  such  as  sometimes  occurs  in  Helminthostarhys. 
'fhe  converse  is  not  tenable  unless  we  accept  the  view  that  the  sterile  leaf  is  an 
older  structure  than  the  sporangiophore,  a  view  which  we  believe  is  not  warranted 
by  the  facts.  It  has  been  suggested  in  a  previous  chapter  that  the  sporophyll  of  the 
Marattiacea  might  be  accounted  for  by  a  theory  of  concrescence  of  the  sporangiophore 
and  sterile  lamina  in  the  Ophioglossaceae.  Ophtoglossum  palmatum,  with  the  two 
series  of  small  sporangiophores  and  broad  leaf  lamina,  is  the  form  which  comes 
nearest  to  such  a  condition.  A  very  serious  objection  to  this  view  was  mentioned, 
however  —  the  fact  that  the  sporangiophore  is  an  adaxial  structure,  whereas  the 
synangia  of  the  Marattiacea  are  always  abaxial  in  their  position. 

Comparing  the  eusporangiate  ferns  with  the  leptosporangiate,  it  is  generally 
conceded  that  the  Osmundacea  are  the  ferns  which  most  closely  approach  the 
Euspoiangiata.  The  Osmundacea  show  points  of  resemblance  to  both  the  Ophio- 
glossacea and  Marattiacea,  this  being  true  both  of  the  vegetative  tissues  and  the 
sporangia.  In  Osmunda  the  arrangement  of  the  sporangia  suggests  Botrycliium, 
while  in  Todea  the  sporangia  are  borne  upon  the  backs  of  the  leaves,  much  as  they 
are  in  the  Marattiacea.  Bower  has  suggested  that  the  Gleicheniacea,  which  are, 
however,  certainly  allied  to  the  Osmundacea  also,  show  certain  suggestions  of  a 
marattiaceous  affinity,  especially  in  the  arrangement  of  the  sporangia. 

We  may  then  briefly  summarize  our  conclusion  as  follows:  From  some  form, 
allied  to  the  simpler  existing  species  of  Ophioglossiirn,  the  whole  fern  series  is 
descended.  In  this  whole  series  the  leaf  is  the  predominant  organ,  the  stem  at  first 
being  quite  subordinate  in  importance.  This  ancestral  fern  was  monophyllous  and 
the  leaf  at  first  was  a  sporophyll,  perhaps  without  any  definite  sterile  segment. 

217 


218  CONCLUSION 

From  this  central  type  presumably  several  lines  diverged,  of  which  only  a  few  frag- 
ments persist.  One  of  these  is  seen  in  the  different  forms  of  Botrychium,  to  which 
Helminthostachys  is  probably  not  very  remotely  allied.  The  whole  of  this  series  is 
characterized  by  a  subterranean  gametophyte,  and  a  more  or  less  saprophytic  habit 
of  the  sporophyte  is  indicated  by  the  development  of  a  mycorrhiza  in  the  roots. 

The  Marattiaceae,  as  they  now  exist,  probably  do  not  represent  a  single  un- 
broken line  of  descent,  and  show  strong  evidences  of  a  possible  multiple  derivation 
from  the  earlier  stock.  The  point  of  contact  with  the  Ophioglossacea;  is  probably 
in  the  neighborhood  of  Helminthostachys,  which,  on  the  whole,  is  more  like  the 
Marattiaceae  than  are  the  other  Ophioglossaceae;  but  it  is  improbable  that  the  solid 
synangium,  such  as  characterizes  most  of  the  Marattiaceae,  was  derived  from  a 
group  of  separated  sporangia  like  those  in  Botrychium  or  Helminthostachys,  and  it  is 
more  likely  that  they  arose  from  a  structure  which  resembled  the  spike  of  Ophio- 
glossum.  Angiopteris  is,  with  little  question,  the  most  specialized  of  the  living 
Marattiaceae  and  has  probably  departed  further  from  the  ancestral  type  than  any 
of  the  other  forms,  while  Kaulfiissia,  on  the  other  hand,  is  probably  the  most 
primitive.  On  the  whole  the  Marattiaceae  are  nearer  to  the  leptosporangiate  ferns 
than  the  Ophioglossaceae  are,  and  it  is  likely  that  the  Leptosporangiates  are  directly 
descended  from  some  ancient  fern  forms,  allied  to  the  Marattiaceae,  but  differing 
from  any  of  the  existing  types. 


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1.  Vergleichende  Untersucliungen,  betrelFend  die  Histologie  der  vegetativen  und  sporenbildenden 

Organe   und   die   Entwickelung   der   Sporen   der   Leitbundelkryptogamen.      Mem.  de 
I'Acad.  imp.  des  sciences  de  St.  Pctersbourg,  1S72,  ser.  7,  19,  no.  i. 

2.  Betraclitungen   uber  das  Leitbundel  und    Grundgewebe  aus  vergleichend  morphologischem 

und  physiologischem  Gesichtspunkte.     Dorpat,  1875. 

3.  Developpement  des  tubes  cribreu.x.     Ann.  des  sci.  naturelles,  1882,  ser.  6,  14,  167. 
Sadebeck,  R. 

I.  Der  Embryo  von  Equisclum.     Bot.  Zeit.,  1877,  44.     Also,  Pringslieim's  Jalirb.  fur  wiss.  Bot., 
1878,  II,  SIS- 

SCHOUTE,  J.  C. 

Die  Stelartheorie.     Groningen,  1902. 
Scott,  D.  H. 

I.  Studies  in  Fossil  Botany.     London,  1900. 

Second  edition,  1909.     (Also  many  monographs  on  fossil  plants.) 
Seward,  A.  C. 

I.   Fossil  Plants.     2  vols.     Cambridge,  1897-1910. 
Shaw,  W.  R. 

1.  The  Fertilization  of  Onoclea.     Ann.  Bot.,  1898,  12,  251-285. 

2.  Ueber  die  Blepharoplasten  bei  Onoclea   und   Marsilia.     Ber.  d.  deutsch.  bot.  Gesell.,  i8g8, 

16,  177-184- 
Shove,  R.  F. 

I.  On  the  Structure  of  the  Stem  o{  Angiopteris  evccla.     Ann.  Bot.,  1900,  14,  497. 
Solms-Laubach,  H.,  Gra^  zu. 

I.  Fossil  Botany.     Oxford,  Clarendon  Press,  1891. 
Strasburger,  E. 

1.  Die  Befruchtung  bei  den  Farnkrautern.         Pringsheim's  Jalirb.  fur  wiss.  Bot.,  7,  390. 

2.  The  Periodic  Reduction  of  Chromosomes  in  Living  Organisms.     Ann.  Bot.,  1894,  8,  281. 

3.  Ueber  Reductionsteilung.     Sitzungsber.  der  K.     Preuss.     Akad.  der  Wiss.,  1904,  18. 
Tansley,  A.  G. 

I.  Lectures  on  the  Evolution  of  the  Filicinean  Vascular  System.     Cambridge,  1909. 
Ternetz,  Charlotte. 

I.  Ueber  die  Assimilation  des  atmosphaerischen  StickstofFcs  dutch   Pilze.     Pringsheim's  Jahrb. 
fiir  wiss.  Bot.,  1907,  44,  353. 
Treub,   M. 

I.  Etudes  sur  les  Lycopodiacees.    Ann.  du  Jardin  botani<iue  de  Buitenzorg,  1884-1890,  4,  5,  7,  8. 
Underwood,  L.  M. 

1.  Our  Native  Ferns  and  their  Allies.     6th  ed.     New  York,  1900. 

2.  A  Review  of  the  Genus  Danaa.     Bull.  Torrey  Bot.  Club,  1902,  29,  669. 
Van  Tieghem,  Ph. 

1.  Sur  quelques  pointes  de  I'anatomie  des  cryptogames  vasculaires.  Bull,  de  la  Soc.  bot.  de  France, 

1883,   25,    169. 

2.  Sur  la  limite  du  cylindre  centrale  et  de  I'ecorce  dans  les  cryptogames  vasculaires.     Journ. 

de  botanique,  1888,  369. 

3.  (and  Duliot)  Recherches  comparatives  sur  I'origine  des  membres  endogenes  dans  les  plantes 

vasculaires.     Ann.  des  sci.  naturelles,  1888,  ser.  7,  t.  8,  i. 

4.  Remarques  sur  la  structure  de  la  tige  des  Ophioglossees.     Journ.  de  botanique,  1890,  365. 
J.  Traite  de  botanique.     2.  ed.  Paris,  1892. 


LIST   OF    PLATES. 

Plate  i. 

1.  Two  spores  o{  Ophioglossiim  moluccanum  Schlecht,  showing  range  in  size,     x  500. 

2.  Two-celled  ganietopliytc  of  0.  molucranum. 

3.  A  three-celled  stage.     sf>,  ruptured  spore  membrane. 

4.  A  four-celled  stage  seen  from  above. 

5.  Two  transverse  optical  sections  of  a  four-celled  gametopbyte. 

6.  Three-celled  gametopbyte  of  0.  intermedium  Ilk. 

7-9.  Young  gametophytes  of  O.  pendulum  L.,  showing  mycorrbizal  infection,     m,  niycorrhizal 
filaments. 
10.  Adult  gametopbyte  of  O.  mo/ufct(fium.     x  10.     ^,  basal  tuber;    5  ,  antberidia. 
H-14.  Gametophytes  of  O.  pendulum.     X  j.     /;,  adventitious  buds;  sp,  young  sporopbytc. 

15.  Upper  part  of  ripe  antberidium  of  O.  pendulum.     X  275.     0,  opercular  cell. 
16-20.  Development  of  the  spermatozoid  in  0.  moluccanum.     x  950.     hi,  blepharoplasts. 

Plate  2. 

21-29.  Spermatogenesis  in  Uphwglossum  pendulum,     x  950.     21  shows  spermatocyte  before  final 
nuclear  division,  with  two  blepharoplasts,  bl ;  22,  23,  nuclear  spindle  from  side  and  pole; 
24-29,  development  of  spermatozoid;  n,  nucleus  of  spermatozoid;  c,  cilia;  v,  protoplasmic 
vesicle. 
30-32.  Three  stages  in  the  development  of  the  archegonium  of  O.  pendulum,  x  275.    i,  basal  cell; 
«',  n",  neck  canal  cells. 
^2-  Venter  of  the  archegonium,  showing  apparently  a  ventral  canal  cell,  v;  n,  one  of  the  nuclei 
of  the  neck  canal  cell,     x  650. 
34-37.  Spermatogenesis  in  B.  virginianum;  38-41,  in  Kauljussia;  42,  43,  in  Damta.     All  x  950. 

44.  Nearly  ripe  spermatozoids  of  Angioptcris.     x  950.     n,  nucleus;  bl,  blcpharoplast;  c,  cilia; 

v,  vesicle. 

45.  Nearly  ripe  archegonium  oi  Danica,  showing  apparent  ventral  canal  cell,  v. 

46-48.  Recently  fertilized  egg-cells  of  Dantea.    sp,  spermatozoid  (?)  within  the  egg-nucleus. 

Plate  3. 

Ophinglnssum  mi>lucciinum  Schlecht. 

Several  types  collected  at  Buitenzorg,  Java,  and  referred  to  O.  moluccanum  Schlecht.    There  are 
at  least  three  species.    Fig.  5  is  the  typical  O.  moluccanum.    All  figures  about  natural  size. 

Plate  4. 

A.  Six   plants  of  Ophioglossum  (Ophiodcrmn)  intermedium   Hk.   reduced   one-half.     Collected   at 

Buitenzorg,  Java. 

B.  Ophioglossum  {Ophioderma)  pendulum  L.,  collected  in  the  Hanuclla  Reserve  I'orest,  Ceylon. 
1,2.  Full-grown  sporophytes  of  0. /)£^ni/u/«m,  much  reduced.    In  2  the  sporangia!  spike,  sp,\s 

forked. 
3-6.  Details  of  the  sporophyll  and  sporangiopborc. 

Plate  5. 

Ophioglossum  (Cheiroglossn)  patmntum  L.,  collected  in  Jamaica. 
I.  The  whole  plant. 
2,  3.  Sporophylls.     In  3  there  is  a  single  median  spike. 

Plate  6. 

A.  I,  Botrychium  obliquum  Miibl.;  2,  B.  lunaria  L. 

B.  B.  virginianum  (L.)  Swz. 

Plate  7. 

Botrychium  stlaijolium  Pr.     California. 


224  LIST    OF    PLATES 

Plate  8. 

A.  Young  plant  o(  Hclmititliostachys  zeyltinitu  (L.)  Ilk.      Rcdiictd  about  onc-lialf. 

B.  Full-grown  plant  oi  Hehninihostachys,  reduced  about  two-thirds.     Collected  in  the   Hanwclla 

Reserve  Forest,  Ceylon. 

Plate  g. 

A.  I,  small  plant  of  Df/Hrcrt  jinmani  Underwood;  2,  rhizome  of  the  same  species;   5,  apt.x  of  sterile 

leaf;  4,  fertile  leaf;  5,  sterile  leaf  of  D.  jamaicensis  Underwood. 

B.  I,  young  plant  of  Danwa  elliptica  Sm.  (.'');  2,  sporophyll  of  D.  jamaicensis;  ^,  4,  very  young 
plants  of/),  jimuiiccnsis  {'>.). 


Plate 


All  specimens  collected  in  Jamaica. 

10. 

Adult  sporophyte  of  Daiuea  illiptun.      Ja 


Kauljussia  ivstulijolia  Bl. 

1.  Young  plant  showing  the  rhizome. 

2.  Sporophyll.     Specimens  collected  near  Buitenzorg,  Java. 

Plate  12. 

A.  Marattia  iilata  Swz. 

1.  Part  of  fertile  leaf. 

2.  A  single  fertile  pinna. 

3.  Fallen  leaf-base  with  adventitious  buds,  k. 

B.  Marattia  alata. 

I.  Leaf  from  young  plant  developed  from  an  adventitious  bud. 
2,  3.  Young  sporophytes  arising  from  fertilization. 
All  specimens  from  Jamaica. 

Plate  13. 

Angiopterts  evecta  (Forst.)  HofFm. 
1-3.  Specimens  from  Australia;  4,  5,  specimens  from  Peradeniya,  Ceylon. 

I,  caude.x  of  a  small  plant;  2,  part  of  a  sporophyll;  3,  cross-section  of  the  petiole  of  a  full-grown 
leaf;  4,  young  sporophyte  arising  from  the  prothallium;  5,  single  leaf  from  a  similar  sporo- 
phyte. 


A-} 


/S 


■c^.^. 


.■\ 


.6 


^^K 

^^m 


1.  Two  spores  of  O.  moluccanum,  showing  range  in  size.  X  500. 

2.  Two-celled  gametophyle  of  O.  moluccanum. 

3.  A  three-celled  stage.     5p,  ruptured  spore  membrane. 

4.  A  four-celled  stage,  seen  from  above. 

5.  Two  transverse  optical  sections  of  a  four-celled  gametophyle. 

6.  Three-celled  gamctophyte  of  O.  intermedium  Hk. 

7-9.  Young  gametophytcs  of  O.  pendulum  L.,  showing  myconhizal 
infection,     m.  mycorrhizol  filaments. 


10.  Adult  gamctophyte  of  O.  moluccanum.    X    10.     /,  basal  tuber; 
3  ,  antheridia. 
11-14.  Gametophytcs  of  O.   pendulum.    X    3.     A,   adventitious  buds; 
sp,  young  sporophytc. 
15.  Upper    part    of    ripe   antheridium    of    O.  pendulum.    X   275. 

16-20.   Development  of  the  spermatozoid  in  O.  moluccanum.      X  950. 
hi,  Itlepharoplasts. 


''^yj^ft*' 


#  „  i 


30-32, 
33. 


Spermatogenesis  in  Ophioglossum  pendulum.  X  950;  21  shows 
spermatocyte  before  final  nuclear  division,  with  two 
blepharoplasts,  hi;  22,  23,  nuclear  spindle  (rora  side  and 
pole;  24-29,  development  of  spermatozoid ;  n,  nucleus  of 
spermatozoid ;  c,  cilia;  V,  protoplasmic  vesicle. 

Three  stages  in  development  of  archegoiuum  of  O.  pendulum. 
X  275.     A,  basal  cell;  n'.  n-',  neck  canal  cells. 

Venter  of  archegonium  showing  apparently  a  ventral  canal  cell,  t). 
n,  one  of  the  nuclei  of  the  neck  canal  cell.    X  650. 


34-37.  Spermatogenesis    in    B.    cirginianum;    38-41,    in   Koulfussia; 
42,  43,  in  Daniea.     All  X  950. 

44.  Nearly  ripe  spetmatozoids  of  Angiopleris.    X  950.     n,  nucleus : 

A/,  blepharoplast;  c,  cilia;  V,  vesicle. 

45.  Nearly  ripe  archegonium  of  Danaa,  showing  apparent  ventral 


ell. 

46-48    Recently  fertilized  egg-cells  of  Da 
within  the  egg-nucleus. 


oid  (?) 


\ 


A.  Six    plants    ot    Ophiogh 

Builenzorg,  Java. 

B.  Ophioglossum  {Ophiodcrma)  pendulum  L.      C. 

1,  2.  Full-grown  sporophylcs  o(  O.  pendulum, 
i-6.  Details  ol  the  spotophyll  and  sporangiophc 


(OpIiioJcrma)    inlcrmedium     Hk.,    reduced 


cted  in  the  Hanwella  Reserve  Forest,  Ceylon. 

ich  reduced.     In  2  the  sporangial  spike,  sp,  is  forked. 


Ophioglossum  {Cheiroglossa)  palmalum  L.     Collected  in  Jamaica. 
I .  The  whole  plant.     2,  3.  Sporophylls;  in  3  there  is  a  single  median  spike 


A.  I.  small  plant  o(  Danaa  jenmani  Underwood;     2.  rhizome  of  the  same  species;    3,  apex  ot  sterile  leaf; 

4.  fertile  leaf;     5,  sterile  leaf  of  D.  Jamaicensis  Underwood. 

B.  I.  young  plant  of  Dancta  MpUca  Sm.;      2.    sporophyll    ot  D.   Jamaican,),:       3.    4.    very  young 

plants  of  D.  jamaicensis  (?). 

All  Specimens  from  Jamaica. 


Adult  sporophyle  of  Dansa  clUptica.     Ja 


Kaultussia  oesculifolia  Bl. 

1,  young  plant  showing  the  rhizome;  2,  sporophyll. 

Specimens  collected  near  Buitenzorg.  Java. 


^^n 


lis 


31 


g  ^ 


X   g 


Library 
N".  O.  State  Gollfl«r« 


INDEX 


Adder-tongue  fern.     See  Ophioglossuni. 
Adventitious  buds.     See  Buds. 
Alternation  of  generations,  209 
Aneura,  120 

•Angiopteris,  4,  117,  118,  120,  121,  126,  139,  140, 
141,  146,  ISO,  152,  153,  154,  IS5, 
158,  164,  196,  198,  199,  201,  202, 
203,  204,  20s,  207 
Figs.  88,  89,  95,  loi,  109,  no,  iii,  112, 
124,  130,  134,  180, 181, 182, 183, 187 
Plate  13 
Angiopteris,  species  of,  196 
Angiopteris  evecta  (Forst.)  Hotfm.,  119 
Angiopteris  pruinosa  var.  hypoleuca,  122 
Annulus  of  sporangium,   208 
Antheridium: 

Angiopteris,  126 
Anthoceros,  42,  122,  211 
Botrychium,  18,  24,  21; 
Danasa,  126,  128 
Equisetum,  24 
Helminthostachys,  20,  21 
Kaulfussia,  127 
Lycopodium,  24 
Marattia,  126,  128 
Marattiaceae,  24,  129 
Ophioglossum,  22,  23,  24 
.■\nthoceros,  Anthocerotes,  42,  122,  210,  211 
Apical  growth.    See  Leaf,  Root,  Stem. 
Apogamy  (in  Botrychium),  52 
Archangiopteris  henryi,  4,  117,  203,  204 

Fig.  184 
Archegonium: 

Angiopteris,  131 
Botrychium,  30,  31 
Danxa,  132,  133,  134 
Helminthostachys,  20,  21 
Kaulfussia,  13 
Marattia,   126 
(Iphioglossuni,  28,  29 
.Archesporium: 

Botrychium,  1 15 
Helminthostachys,  111; 
Marattiaces,  206 
Ophioglossum,  115 
Asplenium  nidus  L.,  10,  13 
Blepharoplast,  26,  128,  129 

Botrychium,  3,  j,  16,  17,  18,  19,  25,  27,  28,  30, 
31,  32,  39.  46,  47.  48,  49.  50,  .S2.  66, 
82,  83,  99,  loi,  102,  103,  109,  no, 
136,  142,  213 
Classification  of,  99 
Botrychium  lanuginosum  Wall.,  99,  loi,  10? 
Fig.  74 


I    Botrychium  lunaria  (L.)  S\v.,  6,  16,  17,  28,  34,  46, 
48,  50,  52,  65,  83,  99,  m 
Fi<;s.  8,  36,  71 
Plate  6 
B.  matricari;cfolium  A.  Br.,  16 
B.  obliquum  Muhl.,  16,  34,  39,  53,  54,  103,  136, 
142 
Plate  6 
B.  silaifolium  Pr.,  99 

Plate  7 
B.  simplex  Hitchcock,  5,  6,  16,  83,  99,  100,  109, 
IIS 
Fig.  71 
B.  ternatum  (Thbg.)  Sw.,  100,  103 

Fig.  71 
B.  virginianum  (L.)  Sw.,  6,  16,  17,  18,  27,  28,  32, 
34.  46.  47.  50.  52,  53,  54.  59.  60, 
61,  63,  67,  69,  83,  99,  100,  loi,  103, 
no,  112,  n4 
Figs,  7,   14.   IS.   17.  28,  29,  32,  33.  40, 
41.  42,  43,  44.  71.  72,  74.  76,  77.  85 
Plate  6 
Botryopterideiv,  3,  214 

Bryophytes   (see  also  Mosses,  Liverworts),  212 
Buds: 

in  Botrychium,  loi 
on  leaf  of  Dan.-ea  sintensis,  178 
on  gametophyte  of  Marattiace*,    121 
on  gametophyte  of  Ophioglossum,  14 
on   primary   root  of  Ophioglossum,   40 
root  buds  in  Ophioglossum  vulgatum,  58,  59 
Calcium  pectate  in  Marattiaceae,  204 
Calcium  oxalate  crystals  in  Marattiacea?,  204 
Cambium,  65,  82 
Canal,   so-called    "canal"   in    Helminthostachys, 

74.  79 
Cauline  fibro-vascular  bundles  (see  also  Commis- 
sural  strand),    174,    175,  184,   191, 
197 
Cheiroglossa  (see  also  Ophioglossum   palmatum), 
5.88 
Fig.  70 
Plate  5 
Chlorophyll  in  gametophyte  of  Ophioglossum,  9, 

Christensenia  =  Kaulfussia,  122 

Collateral  bundles,  Primitive  nature  of,  214 

CoUenchyma  in: 

Angiopteris,   202 

Kaulfussia,  186 

Marattia,  194 
Commissural  vascular  bundles  in — 

Angiopteris,  197 

Dan:ca,  174,  175 


226 


Commissural    vaseular   bundks  in — 
Marattia,   191 
Kaulfussia,    184 
Commissure  (of  stipules),  187 
Completoria  complens,  22 
Corallorhrza,  }} 
Cotyledon  of  — 

Angiopteris,  146,  147,  151 
Botrychium,  50,  51,  52,  64,  67,  8j 
Danaea,  148,  150 
Helminthostachys,  54,  69 
Kaulfussia,   1 47,   149 
Marattia,  138,  147,  150,  151 
Ophioglossum,  35,  42 
Crystals.     See  Calcium  oxalate. 
Cycads,  30 

Dana?a,  47,  53,  82,  84,   117,  iiS,  124,  125, 
128,   135,   142,   151,   154,   160, 
164,  205,  212 
Danaea  elliptica  Smith,  124,   125,  126,  132, 
142,  148,  154 
Figs.  92,  93,  103,  los,  117,  125,  131, 
147,    151,    152,    161.      Plates  9, 
D.  jamaicensis  Underwood,   124,   126,  136, 
144,  146,  148,  154,  155,  156 
Figs.  91,  93,  98,  99,  100,  104,  114, 
116,   118,   119,   120,   121,   125, 
138,   140,   143,   144,   145,   146, 
149,  150,  153,  160,  161,  189 
Plate  9 
D.  jenmani  Underwood,  124 

Figs.  91,  154,  15s,  156,  137,  162 
Plate  9 
D.  simplicifolia  Rudge,  124,  127,  136,  142, 

160,  175,  176,  206 
D.  sintensis,  178 
D.  trichomanoides  Spruce,  178 
Dehiscence  of  — 

Antheridium,  24,  2;,  129 
Sporangium,  109 
Synangium  of  Marattiaceae,  207 
Dichotomy  of  — 

Prothallium  in  Marattiacea",  121 
Root  in  Ophioglossum,  93 
Dicotyledons,  65 
Dictyostele  in  — 
Angiopteris,  197 
Dana;a,  175 
Kaulfussia,  185 
Marattia,  192 
Drosera,  32 
Embryo  of  — 

Angiopteris,  139 
Botrychium,  46,  47,  48,  51.  136 
Danaea,  118,  136,  142 
Helminthostachys,   54,  67 
Kaulfussia,  141 
Marattia,  13;,  136,  137 
Marattiacea?,  118,  135 
Ophioglossum,  34,  35,  36,  37,  38,  43 


Endodermis: 

Angiopteris,  164,  201 

Dan^a,  163,  167 

Helminthostachys,  72 

Kaulfussia,  164,  182,  183 

Marattia,  164,  193 

Ophioglossum,  92 
Endarch  bundles  in  Helminthostachys,  77 
Endophyte.     See  Mycorrhiza. 
Entomophthoreie,  22 

Eqiiist  tLim,  KiiuisL-tinea",  26,  27,  39,  132,  139 
Eubotrychiuni  (see  also  Botrychium),  100 
Euophioglossum  (see  also  Ophioglossum),  83, 

86,  89,  91,  93 
Eusporangiatae,  3 

Comparison  with  Bryophytes,  209,  210,  212 

Nature  of  vascular  system,  214 

Relation  to  Leptosporangiatx,  217 
Fegatella,  33 
Ferns,  origin  of,  209 
Fertilization: 

Botrychium,  32 

Marattiaceae,  134 

Ophioglossum,  31 
Fibro-vascular  system  (see  also  Leaf-trace,  Stele) : 

Angiopteris,  196,  198,  199,  201 

Botrychium,  60,  62,  66 

Danxa,   160,    162,   163,    164,    166,    I.72,    174, 
.76 

Helminthostachys,  73,  76,  77,  78,  106 

Kaulfussia,  181,  182,  184,  185 

Marattia,   189,   191,   193 
Fossils: 

Bryophytes,  209 

Ferns,  3 

Marattiaceae,  117 
Gametophyte: 

Angiopteris,  121 

Botrychium,  16,  17,  18 

Danaea,  124,  125 

Helminthostachys,  20,  21,  22 

Kaulfussia,  122,  123 

Marattia,  119,  121,  122,  210 

Ophioglossum,  6,  10,  11,  12,  13,  14,  15,  211 
Germination  of  spores: 

Marattiace;e,  119,  1 20 

Ophioglossaceae,  7,  8,  9 
Gleichenia,  mycorrhiza  in,  33 
Gymnogramme,  26 
Hairs: 

Marattiaceae,  1 50 

Ophioglossum  palmatum,  99 
Helminthostachys,  5,  8,  10,  19,  20,  21,  25,  31,  32, 
54,  67,  68,  69,  70,  71,  72,  73,  74,  75, 
76,  77.  78,  79,  80,  81,  82,  84,  104, 
103,  106,  107,  108,  112,  115,  116, 
213.  214 
Figs.  10,  1 1,  45,  46,  47,  48,  49,  50,  51,  52, 

53,  54,  78,  79,  80,  86 
Plate  8 


227 


Horned  liverworrs   (sec   also  Antliocerotes) 

209 

Indusium,  204 

Isoetes,  205,  206 

Kaulfussia,  4,  82,  84,  117,  118,  119,  122 

123 

132, 

141,   147,   149,   152,   153, 

154. 

iSS, 

157,   158.   164.   178,   179. 

180, 

181, 

182,    183,   185,   186,   187, 

206 

208 

Fifts.   90,  96,    102,    113,    123, 

128, 

I3f', 

141,   163,   164,   166,   167, 

168, 

170, 

171,  1S8 
I'l  ire  1  I 

Laeiin;c: 

Intcrnodal   in   1  lelniinrliostaelns. 

75 

Inrernodal  ,n   Kaulfussia,   .84 

Leaf; 

Ansiopf^ii^.  -01 

l^otrychium,  61,  loi 

Danaea,  176,  178 

Helminthostachys,  67,  70,  74 

Kaulfussia,  185 

Marattia,  194 

Marattiaceae,  118,  157,  159,  214 

Opliioglossum,  57,  84,  87,  88 

Leaf,  anatomy: 

Angiopteris,  202 

Botrvchium,  102 

Danxa,  160 

Helmintliostacl)\s,  107 

Kaulfussia.   187 

Marattia,  194,  195 

Opliioglossum,  93,  96 

Leaf,  ferrile  (see  also  Sporopliyll),  5,  85, 

109, 

204, 

-:i,l 

Leaf,  gaps,  78,  173 

Leaf,  trace,  66,  72,  80,  173,  186,  191,  197 

Leptosporangiata?,  3,  217 

Liverworts,  mycorrliiza  in,  33 

Lycopodium,  9,  10,  24 

L.  cernuum,  9,  10 

Mantle  cells  (of  antheridium),  24,  129 

Marattia,  117,  119,  120,  122,  126,  128, 

132. 

I3S. 

136,   137,   147.  149,  152. 

IS3. 

15  s. 

156,   164,   188,   189,   192, 

193- 

194. 

195,  204,  206 

M.   alata   Swartz,    138,    188,   191,    192, 

193. 

194 

Figs.  175,  176,  177.      Plate  12 

M.  cicutasfolia  Klf.,  119,  132,  136 

M.  douglasii  (Pr.)  Baker,  119,  120,  122, 

126, 

I3S, 

136,  137,  147,   149,   151, 

53, 

56, 

188,  189,  190,  205,  210 

Figs.  87,  88,  94,  106,  107,  108, 

122, 

27.    1 

13^   13.3.   14''   "7i.   171. 

74- 

77. 

IS:;,  190,  191 

M.  fraxinea  Sniiih,  120,  18S,  igi,  i,,. 

Figs,   87.    186 

M.  salicifolia  Schrad.,  193 

M.  sanibucina  Blunie,  120,  188 

FiK.  87 

M.  weinmannixfolia  Liehm.,  136 

Marattiacea?,  3,  35,  39,  48,  53,  61,  83,  84,   117, 
129,   130,   134,   135,   209,   212,   214, 

215 

Macroglossum,  117,  204 
M.  alidie  Copeland,  204 
Mesarch  vascular  bundles  in  I  lelininrliosraclns, 

78 
Monotropa,  33 
Mosses,   209 

Mucilage  cells,  168,  170,  173,  177,  182,  185,  187, 
I  190 

j    Mucilage  ducts,  168,  170,  173,  177,  182,  185,  187, 
190 
Mycorrliiza,  6,  9,  II,  15,  18,  19,  20,  21,  22,  32, 

33,127,179,181,212 
Operculum    (of  antheridium),   24,    25,    128,    129 
j    Ophioderma  (see  also  Opliioglossum),  5,  87,  94 
I    Ophioglossacea;,  3,  5,  6,  7,  34,  82,  86,  108,  109, 
208,  213,  214 
Ophioglossum,   5,  6,  7,  9,  10,  11,  12,  13,  14,  15, 
22,  24,  26,  27,  28,  35,  39,  42,  43,  56, 
60,  82,  83,  85,  86,  87,  89,  91,  207, 
209,210,213,214,215 
O.  bergianum  Schlecht,  5,  87,  92 
O.  capense  Sw.,  92 
O.  californicum  Prantl.,  5 
O.  ellipticum  Hk.,  92 
O.  intermedium  Hooker,  88,  97, 
Fig.  69 
Plate  4 
O.   lusitanicum   L.,   86,   87 

O.  moluccanum  Sclilecht.,  5,  6,  7,  11,  12,  26,  28, 
34-  35-  36,  38,  39.  40,  42.  45.  55. 
56.  57.  59-  86,  90,  94,  1X2,  210,  212 
Figs.  2,  4,  12,  18,  22,  23,  24,  2c;,  26,  27, 
37.  38,  39,  55.  56,  57.  58.  59.  60,  61. 
62,  81,  83,  192 
Plates  I,  3 
O.  palniatum  L.,  88,  89,  98,  99 
Fig.  70 
Plate  5 
O.  pedunculosuni  l)es\-.,  10.  n.  13,  34,  36.  39.  40, 
42.  57 
Fig,  3 
O.  penduhuii  L.,  5.  6.  7.  9,  10.  14.  18,  26.  28.  29, 
36,  37,  38.  40,  42,  44,  56,  88,  95,  96, 
109,  112 
Figs.  I.  3,  4,  13,  16,  20,  21,  63,  64,  65,  66, 

67,  68,  82,  84 
Plates  I,  2,  4 
O.  reticulatum  L.,  6,  40,  90 
O.  simplex  Ridley,  88.  98,  109 

Fig.  71 
O.  vulgatum  L..  3.  5.  6.  10.  13.  15,  27,  28,  2<>,  34, 
43.44,57.58,59.86,87,92 
Figs.  3,  5,  19 
Orchids  as  humus  saprophytes,  33 
Osmunda,  Osmundaceae,  121,  123.  207 
Osmundopteris.     See  Botrychium  \irginianum. 
Pali.sade  tissue,  107,  178.  195,  202 


228 


Pellia,  122 

Periderm,  66,  8o,  193 

Peronosporeae,  22 

Phyllotrichium  (see  also  Botrychium),   100,  102 

Pith,  in  Helminthostachys,  76,  79 

Polypodium  quercifolium,  10 

Prothallium.     See  Gametophyte. 

Pro-ophioglossum,  211 

Protocorm,  53 

Protophloem  in  Angiopteris,  201 

Protostele,  175,  188 

Protoxylem: 

Angiopteris,  201 

Helminthostachys,  79,  82 

Kaulfussia,  185 
Pteris  cretica,  53 
Pythium,  22 
Rhizoids: 

Botrychium,  18 

Danrea,  127 

Helminthostachj's,  20 

Kaulfussia,  123 

Ophioglossum,  12 
Rhizome  (see  also  Stem) : 

Botrychium,  loi 

Dansa,  175,  176,  177 

Helminthostachys,  106 

Kaulfussia,  186 

Ophioglossum,  91,  94 
Root: 

Angiopteris,  140,  202,  203 

Botrychium,  47,  51,  64,  103,  104 

Danaea,  157,  164,  177,  179 

Helminthostachys,  70,  80,  81,  105,  107,  108 

Kaulfussia,  187' 

Marattia,  138,  156,  192,  195 

Ophioglossum,  35,  39,  43,  56,  83,  87,  89,  93, 
97>98 
Root  apex: 

Botrychium,  49 

Danaea,  178 

Helminthostachys,  72,  80 

Marattia,  138,  156,  195 

Ophioglossum,  94 
Root  hairs,  multicellular,  of  Kaulfussia,  183,  187 
Scales,  epidermal: 

Danaea,  151 

Helminthostachys,  74,  75 

Kaulfussia,  180 

Marattiaceae,  150 
Sceptridium.     See  Botrychium  obliquum. 
Sclerenchyma,  170,  171,  194 
Secondary  wood: 

Angiopteris,  204 

Botrychium,  65,  82 

Helminthostachys,  78 
Sex-organs.     See  Antherldium,  Archegonium. 
Sieve  tubes,  151,  163,  201,  202 
Siliceous  deposits  in  Marattiaceae,  204 


Siphonostele: 

Angiopteris,   197 

Kaulfussia,  184 

Marattia,  188 
Spermatogenesis: 

Botrychium,  28 

Marattiaceae,  129,  130 

Ophioglossum,  26,  27 
Spermatozoids: 

Botrychium,  28 

Marattiaceae,  130 

Ophioglossum,  26,  27 
Spike  of  Ophioglossaceae.     See  Sporangiophore. 
Sporangium  (see  also  Synangium): 

Angiopteris,  205 

Botrychium,  109,  III,  1 14,  1 15 

Danaea,  205,  206,  207 

Helminthostach)'s,  iii,  116 

Kaulfussia,  207 

Marattia,  205 

Ophioglossum,  109,  in,  113 
Sporangiophore: 

Botrychium,  109,  no 

Helminthostachys,  105,  106 

Ophioglossaceae,  5,  85,  108,  109,  208 

Ophioglossum,  109,  no 
Spore: 

Marattiaceae,  208 

Ophioglossaceae,  6,  7 
Spore  division,  114 
Sporophyll: 

Angiopteris,  204,  206 

Archangiopteris,  204 

Botrychium,  100,  102 

Dan«a,  204 

Helminthostachys,  in,  116 

Kaulfussia,  204,  208 

Marattia,  204 

Marattiaceae,  204,  208,  214 

Ophioglossum,  85,  88,  93,  109,  no,  112,  214 
Sporophyte  (see  also  Embryo) : 

Angiopteris,  196,  198,  199,  20l 

Botrychium,  ji,  59,  60,  62,  63,  99 

Danaea,  163,  178 

Helminthostachys,  54,  67,  68,  77,   104,   105 

Kaulfussia,  179,  180,  186 

Marattia,  188,  189 

Ophioglossaceae,   comparison  of  young  spor- 
ophyte, 82 

Ophioglossum,  38,  39,  44,  45,  55 
Staubgrijbchen  of  Marattiaceae,  204 
Stele: 

Botrychium,  82 

Helminthostachys,  52,  75,  82 
Stem,  stem  apex: 

Angiopteris,  153,  198,  199 

Botrychium,  49,  53,  loi,  103 

Danaea,  118,  136,  156,  170 

Helminthostachys,  70,  71,  74 

Kaulfussia,   185,   187 


229 


Stem,  sttm  apex: 

Marattia,   192 

Marattiaceae,  154,  162 

Ophioglossum,  42,  50,  56,  89,  91,  94,  97.  99 
Sterilization  of  sporogenoiis  tissue,  209 
Stipule,  stipular  sheath: 

Botrychium,  6l,  loi 

Dan;ea,  170 

Helminthostachys,  71,  73.  105 

Kaulfussia,   185,   187 

Marattia,  195 

Marattiacex,  118 

Ophioglossaceae,  83,  84 

Ophioglossum,  91 
Stomata: 

Botrychium,  loi 

Dan^ca,  151 

Helminthostachys,   106 

Kaulfussia,  152,  187 

Marattia,  195 

Ophioglossum,  96 
Suspensor: 

Botrychium,  47,  48,  53,  136 

Danaea,  118,  136 


Synangium,  204,  205,  206,  207,  20 
Tannin  cells: 

Angiopteris,  146 

Dannea,  165,  169,  171 

Helminthostachys,   79,   84 

Kaulfussia,  185 

Marattia,  189 

Marattiaceae,  150 
Tapetum,  ill,  116,  206 
Trabeculae,  207 
Tracheary  tissue: 

Angiopteris,  201 

Botrychium,  66 

Helminthostachys,  68,  79,  82 

Kaulfussia,  185 

Marattia,  189 
Ventral  canal-cell,  30,  31,  133.  I34. 

201,  213 
Vestigial  leaves: 

Botrychium  lunaria,  51 

Helminthostachys,  69,  81 

Ophioglossum  vulgatum,  35 


176,  187,  194, 


